Whence the demise and fall of the RNA World?

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Anna Medvegy, Oleg Abramov, Barbara Kremer, Stephen Mojzsis This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-9212823/v1 This work is licensed under a CC BY 4.0 License Status: Under Revision Version 1 posted 10 You are reading this latest preprint version Abstract The RNA World is an early developmental stage in biology before the DNA World. If the first life on Earth began as a cellular RNA life-form which later transitioned to a ribonucleoprotein (RNP) organism, it did not stay that way for long. The last universal common ancestor (LUCA) of all contemporary DNA life seems to have existed already by the late Hadean eon (ca. 4.2 Gyr ago). Understanding what could have driven the evolution of the RNA/RNP World to the DNA World at this early time necessitates a biogeodynamic contextualization of the co-evolution of life and the Hadean Earth environment. Here we draw a connection between recent findings about LUCA and its habitat to make inferences about the earliest biological entities. We argue that environmental conditions on Hadean Earth motivated the transition to a DNA world. Selection pressures on minimalist autonomous RNA/RNP protocells with ribozyme-driven heterotrophic or nascent autotrophic metabolisms favored stability and fidelity. Our findings do not preclude RNA or RNP organisms at the time of the LUCA. Short description A swift demise of the RNA World underscores the hardiness of early life on Hadean Earth rather than its vulnerability to extinction. Biological sciences/Ecology Earth and environmental sciences/Ecology Biological sciences/Evolution Biological sciences/Genetics Biological sciences/Molecular biology RNA World RNP World Origin of Life Last Universal Common Ancestor Hadean Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Introduction Life on Earth is ancient. The prevailing idea has long been that abiogenesis – the prebiotic chemical progression from non-living to living biochemistry – could not have occurred until the early Archean eon by which time Earth’s surface stabilized after the cessation of late accretion bombardment and reduction of high internal heat approximately 3.8 Gyr ago 1 . Growing evidence, however, suggests that conditions on Earth were suitable for life already in its first few hundred million years, during the preceding Hadean eon (4.5-4.0 Gyr ago). Indeed, molecular phylogenetic analysis points to the common ancestry of DNA-protein-based cellular life and the emergence of the Last Universal Common Ancestor (LUCA) by about 4.2 Gyr ago 2 . Analysis also shows that the LUCA was relatively sophisticated; it was part of a microbial population that included an anaerobic acetogen which had by then invented both protein translation and a simple immune system. These features point to a long pre-history for biology on the Hadean Earth 3 . While it remains unquantified how long it took for abiogenesis to occur, the window of opportunity for it to happen continues to narrow (Fig. 1 ). If we accept the argument that life’s inception coincides with the onset of the fundamental ancestor-descendent relationship that defines Darwinian evolution 4 , then the origin of Darwinism requires the origin of biologically useful information in the form of a functional genetic code 5 . This eventuality necessitates the establishment of a molecular genetic lineage allowing for heritable variation of a population to be sorted by natural selection without anticipation. Once this informational threshold is crossed, we take the view that an otherwise proto-biological system can be considered alive when it combines the key properties of information, metabolism and encapsulation together into a functional biont 6 . That said, well before the central role of DNA appeared in biology, there likely existed a precursor RNA World 7 – 9 wherein biologically useful information for life started off with a chiral 10 RNA information-storage molecules which could copy themselves by catalyzing their own replication without the need for other RNAs or peptides. First hypothesized by Woese, Crick, and Orgel in the 1960s 11 – 13 , support for the RNA World was bolstered by the discovery of ribozymes showing catalytic properties 7 , 8 , 14 . A proposed intermediate stage in early life, the RNA+peptide (ribonucleoprotein; RNP) world, posits that proteins became the catalysts of life at some time before DNA took a central role 15 . Once DNA overthrew the RNP world, then contemporary biochemistry began. While this simple scenario remains a rudimentary theoretical account for what was undoubtedly an astoundingly complex sequence of events, the RNA ◊ RNP ◊ DNA model which includes metabolism and encapsulation at the same time, serves as a useful starting point to guide research in the nature and function of the first biomes and their environment. A crucial aspect hanging this argument together is that RNA is capable of autocatalysis in some cases wherein the product acts as the catalyst of its own reaction 16 . The origin of informational and functional RNAs may or may not be different from the origin of encapsulation by proto-cells with some kind of proto-metabolism if these formed together, not in isolation, but as a community. Furthermore, we are reminded of the fact that complete living cells are overall exergonic chemical reaction networks, whereas RNA alone (at least, at present) is a chemical structure with the sole function of making protein 17 . The veracity RNA World hypothesis continues to be a topic of healthy debate 18 , and to better understand its potential origin and eventual demise we must consider the global environment in which it arose on the Hadean Earth. Understanding the early geodynamic evolution of Earth frames our view of the RNA World and the factors driving the transition to a DNA World. The fact that the LUCA was an outcome of Hadean biogeodynamic processes compels us to ask: What kind of life was an RNA organism? What Hadean environments did it inhabit? What metabolic styles did it employ? If the RNA World ever existed as an operative biosphere, why then did the RNA-to-RNP-to-DNA World transition happen at all? Could there be extant RNA or RNP organisms in the present DNA biosphere? Are RNA viruses metaphorically part of the RNA World? A geologically early (ca. 4.3 Gyr ago) time for the events in Fig. 1 appears to be at odds with long-standing biological assumptions about the Hadean environment and the tempo of life’s origin 19 . Here we present a biogeodynamic analysis that reconciles molecular clock phylogenies for the LUCA with Hadean Earth geodynamics to address questions about how the first life forms led to the LUCA. In doing so, we absolve several misperceptions about the survival potential of the emergent biosphere on Hadean Earth. Planetary surface conditions for the RNA World Up to now, attempts to place a time frame on when the origin of life could have occurred were hampered by lack of evidence regarding the nature of the Hadean environment and its ability to host sustained and productive prebiotic chemistry. Developments in the last two decades, however, have radically changed our view of primordial Earth from a dry and unproductive hellscape to one eminently suitable for the kinds of chemistry that could support the origin of the RNA World 20 . Evidently, if life arose so early, then its origin also predates the terrestrial rock record that would otherwise provide key clues about its natural environment 2 . The oldest rocks on Earth are found in the ca. 3.96–4.06 Gyr old Acasta Gneiss Complex in Canada. Regrettably, the polyphase metamorphic Acasta rocks reveal little about prevailing surface environmental conditions 4 Gyr ago 21 . That is because the granite/granitoid protoliths of these gneisses formed in the mid-crust, not at or near the surface. Owing to a long residence time, the Acasta rocks are now expressed as a complex suite of migmatites interleaved with (older) enclaves of hornblende-plagioclase schists 22 . Such rocks do not form anywhere near where biochemistry takes place and hence contain no record relevant to it. Rather, sediments formed in liquid water such as shales and chemical precipitates (e.g. banded iron formations) are the best sources of information about environmental conditions in deep time. At the present, however, there are no agreed-upon Hadean rocks of sedimentary origin on Earth that could potentially yield such information about surface conditions at the time of life’s emergence. We must rely on other sources of information. Extending a direct analysis > 4 Gyr into time means that we must turn to information gleaned from tiny (< 1 mm) ancient detrital zircon (Zr(SiO4)) crystals as old as 4.4 Gyr found in younger sedimentary rocks from Western Australia and South Africa 23 , 24 (Fig. 2 ). Aside from isotopic and trace element geochemical data which appear to indicate that Hadean crust interacted with liquid water and that this crust included some inventory of continental affinity, a very few of these oldest zircons also host inclusions of isotopically light carbon that may point to a biosphere at 4.10 Gyr ago 26 . Although intrinsic conditions for the origin of life indicated by the oldest zircons – such as a stable crust and hydrosphere – appear to be favorable for an early origin, important extrinsic effects unique to the Hadean Earth such as intense late accretion bombardment by comets, leftover planetesimals and asteroids were an important limiting factor. Clearly, conditions on a planet’s surface must remain favorable long enough, somewhere, for prebiotic chemistry to develop into self-sustaining biology. Otherwise, without such conditions the system will experience an early failure, potentially thwarting any chance for life to take hold. Results Exogeneous selection pressures A firm upper temporal limit for the origin of life on Earth is imposed by the giant impact hypothesized to have formed the Moon. This event is proposed to have happened after a planetary object of at least Mars-mass (diameter ca. 6800 km) dubbed Theia collided with the proto-Earth at ca. 4.51 Gyr ago 27 . Moon formation was enough to melt crust and mantle rocks down to several hundred kilometers depth, thus eliminating any chance for survival of a nascent biosphere before that time. Another less well-known boundary condition is provided by the postulated Late Veneer event which may have occurred somewhat later at ca. 4.48 Gyr ago 28 , 29 . This strike was less intense but nevertheless devastating as it may have involved a lunar-sized object (termed Moneta ) which delivered the final ~ 0.5–1% of Earth's mass in inner solar system chondritic material, and as a result enriched the terrestrial mantle in highly siderophile elements such as Ir, Pt and Pd at chondritic relative proportions. The rule of thumb for impacts of such magnitude is that they lead to wholesale crustal melting with associated magma oceans of varying depth depending on the mass of the impactor. During post-impact cooling that follows such colossal events, atmospheric greenhouse forcing plays a critical role in regulating magma ocean lifetimes, which range from ~ 30 to ~ 500 Myr depending on volume of magma, redox conditions, and volatile inventories. Under rapid cooling scenarios, a quasi-steady-state global radiative equilibrium state can be reached as early as ~ 2 Myr post-Moon formation 30 . Some models for the timelines of magma ocean cooling show that extended windows for clement surface conditions are feasible if cooling times are relatively rapid, such as that expected for a Late Veneer scale impact (e.g. ≤1000 km diameter). This insight may help reconcile the rapid origin of life with phylogenetic estimates for LUCA. Furthermore, that Hadean zircon data seem to indicate a hydrosphere has been present on Earth since ca. 4.4 Ga, would also imply an atmosphere to maintain pressure to keep water liquid. This interdependence of the timing of the last wholesale crustal melting event and subsequent stabilization of the surface to allow prebiotic chemistry to take place underscores how conditions on the Hadean Earth set the stage for the RNA World's brief tenure. Moreover, dynamical models of planet formation linked to asteroidal meteorite ages 31 and cratering statistics also show that conditions conducive to prebiotic chemistry were in place on Hadean Earth before 4.2 Gyr ago 5 . Different thermal models that have been reported for the effects of impact bombardments have their limitations, but all agree that there are no obvious barriers to life on Earth for most of the Hadean eon. Previously, it was assumed that an episode in late accretion termed the late heavy bombardment (LHB) at 3.8–3.95 Gyr set a maximum temporal limit on the origin of a persistent biosphere 1 . It is now understood, however, that linking the lunar cratering record with returned Apollo samples is biased by collection on the lunar near side that was extensively modified by Imbrium basin ejecta 32 . Modern models for late accretion of leftover material from planet formation 33 , 34 , extended to earlier times (4.5 Gyr), generally show that late accretion may even have supported life’s emergence (Fig. 3 ). This new view combining information from the Early Earth geology and estimates of the mass flux of impactors over time including the Late Veneer, is also important to the recent formulation of the so-called Discontinuous Synthesis Model 35 . This model argues that oligomeric RNA was actively produced on Hadean Earth’s surface thanks to one or more transient reduced (H 2 -rich) atmospheres formed via reaction between metallic iron (Fe 0 ) from accreting asteroids or planetesimals with surface water or oxidized mantle, or both 29 . These early transient H 2 -rich atmospheres were productive sources of prebiotic chemistry before the impact flux waned in the late-Hadean (ca. 4 Gyr ago), by which time life on Earth was in full swing. Endogenous selection pressures According to the geologic record and planetary dynamical models of late accretion, Hadean Earth could begin to host life. Already by that time the planet possessed liquid water, simple organic molecules, and free energy from chemical disequilibria. These, and enough time for relatively quiescent surface conditions to become established, allowed for both productive and sustained prebiotic chemistry to happen. A further outcome of late accretion's impact flux was to boost supply of exogenous organics and volatiles, such as water, phosphate and carbon compounds to the surface zone to help feed prebiotic chemistry 36 . Recent progress in geochronology, isotope geochemistry, and mineral chemistry of the Hadean terrestrial zircons also shows evidence for emergent land and a functioning hydrological cycle by about 4.0 Gyr ago. Specifically, low 18 O/ 16 O oxygen isotopic values in detrital zircons collected from the Jack Hills of Western Australia and the Barberton Greenstone Belt in South Africa, attest to interactions between meteoric freshwater and crust that in turn implies the presence of exposed landmasses, rainfall, catchment and weathering processes 37 . Taken together, the primordial establishment of a dynamic crust-hydrosphere-atmosphere interface means that environments allowing for prebiotic chemistry, such as wet-dry cycles in shallow ponds or hydrothermal systems on land 38 and fed by local prebiotic chemical reactors were present to concentrate reactants and promote the assembly of RNA precursors, protocellular structures and focus accumulation of other environmentally-processed prebiotic molecules. Also, zircon trace-element and isotopic data, analyzed via machine learning reconstructions of parental magmas, show that Hadean crust already contained significant felsic components composed of tonalite-trondhjemite-granodiorite suites and potassic granites formed through shallow-depth partial melting at convergent plate margins 39 , 40 . The significance of such a geodynamic setting is that it promotes crustal stabilization and volatile recycling, that in turn enhances the availability of disequilibrium chemistry to drive chemical complexity at the global scale 41 . This feature of planetary-scale redox linking the transfer of electrons from mantle to crust to hydrosphere to atmosphere is the geochemical basis of what makes Earth a biocompatible planet. With the planetary dynamics modeling and the late accretion impact flux estimates cited above, we can begin to parameterize what features the first metabolic styles could have had 42 and the relationships of these to the earliest geologic stages of our planet’s evolution. The pre-DNA biome in context Building on the geodynamic and geochemical framework outlined above, we now return to the idea that the very first lifeforms were simple encapsulated RNA-based entities. Unlike modern cellular life, which integrates DNA, RNA, and proteins in a highly interdependent system, a hypothesized RNA organism would have been a minimalist self-replicating unit, potentially consisting of one or a few RNA strands capable of template-directed replication and rudimentary catalysis, captured within a porous proto-cellular structure 43 . The core attributes of such an RNA organism stem from RNA's inherent versatility. Key to the RNA World argument is that experimental reconstructions show that RNA can form ribozymes - enzymatic RNAs - that catalyze their own replication, albeit with low fidelity and efficiency 44 . This autocatalytic capacity would have enabled the steps toward Darwinian evolution to take place in a prebiotic setting through heritable variation arising from replication errors, initially without the need for a separate translation apparatus 4 . Chirality is another pivotal requirement for stable RNA folding and function 10 , and was established early perhaps via prebiotic mechanisms such as asymmetric photolysis or mineral templating 45 . We emphasize encapsulation as a crucial component of this first living system and likely occurred with lipid vesicles or coacervates formed from amphiphilic molecules delivered by impactors or atmospheric chemistry and/or hydrothermal activity. The importance of encapsulation rests on the necessary compartmentalization to maintain chemical gradients and protect against dilution or degradation 43 , 46 . The first entities structurally resembled primitive protocells, but with RNA directing simple polymerization reactions and without the complexity of LUCA's ribosomal machinery. RNA viruses are not the same as the RNA World organisms Next, we draw a key distinction between hypothetical ancient cellular RNA organisms and modern RNA viruses. To be clear, RNA viruses are obligate intracellular parasites that hijack host cellular machinery for replication and lack independent metabolism 47 . The dearth of independent metabolism leads in part to the general consensus that viruses are not life forms. Phylogenetic analyses also suggest that RNA viruses emerged later, possibly as escaped genetic elements from DNA-based cells, rather than as relics of the RNA World 48 , 49 . This evolutionary divergence highlights the point that viruses do not serve as direct analogs for early RNA life, as they exhibit derived features like capsid proteins and host-specific adaptations not present in pre-LUCA scenarios. Pseudo-heterotrophy in the RNA World Instead of being virus-like, primordial RNA organisms were autonomous, proto-cellular systems capable of some kind of metabolism to sustain themselves in Hadean environments through direct interaction with geochemical resources and without relying on pre-existing cells. This is an important distinction; if the first RNA organisms were not autotrophic, neither could they have been heterotrophic sensu stricto . We refer here to the idea of such a simple and early passive “metabolism” for the first RNA life as pseudo-heterotrophic . This term recognizes the reliance of the first organisms for growth and reproduction on the availability of background abiotic production of organic molecules and building blocks generating in the Hadean environment. In these environments RNA World organisms may have been either free-living or attached to mineral or (rock) glass surfaces, or both. Proposed sequence of events Figure 4 schematically reviews the key deviations between the different evolutionary stages of the emergent biosphere: RNA World (Hypothesized origin): RNA was the primary information molecule, acting as both genotype (information storage) and phenotype (catalytic ribozymes). It is characterized by low stability and error-prone replication. RNP World (Ribonucleoprotein transition): RNA acted as a scaffold, recruiting amino acids/proteins to enhance stability and catalytic efficiency, forming complex ribonucleoprotein structures. This allowed for the early translation of genetic code. DNA World (Contemporary life): DNA replaced RNA as the primary, more stable, double-stranded genetic material, allowing for larger genomes, while proteins took over catalysis. DNA is distinct due to deoxyribose sugar and the base thymine. A contemporary RNA/RNP hidden biosphere? Could extant RNA or RNP organisms still be lurking around in the present biosphere? Despite extensive metagenomic surveys of diverse environments - from deep-sea vents to human microbiomes - no evidence exists for separate and independent RNA-based cellular life somewhere in the background of the biosphere 50 . That said, few if any targeted searches have been conducted to search for such organisms. We recommend that such searches be undertaken. Recent discoveries, such as obelisks - short, circular RNA elements associated with bacterial hosts in the human gut - represent virus-like entities but depend on microbial cells for propagation and do not constitute autonomous organisms. Similarly, viroids, which are naked RNA pathogens of plants, lack coding capacity and require host polymerases 51 . The persistence of some kinds of RNA World remnants is instead evident in conserved cellular components, such as ribozymes in the spliceosome and RNase P, and the RNA-centric core of the ribosome all which hint at an ancient RNA-dominated phase 52 , 53 . The absence of extant RNA cells aligns with selective pressures favoring the RNA-to-DNA transition, as RNA's chemical instability – most importantly due to its 2'-hydroxyl (2’-OH) group rendering it prone to hydrolysis – would have limited long-term viability in evolving biospheres 54 , 56 . This conceptualization of a (proto)cellular RNA organism as a transient, rudimentary precursor sets the foundation for exploring Hadean environmental constraints and metabolic innovations that likely shaped its existence and eventual replacement. Chemical vulnerabilities of the RNA/RNP World The hypothetical RNA organisms described in the preceding section, characterized by reliance on RNA for both information storage and catalysis, were sensitive to the physicochemical conditions of the Hadean Earth. While the geodynamic models and geochemical evidence outlined earlier indicate that biocompatible conditions - with liquid water, organic precursors, and energy gradients - were established before 4.3 Gyr ago, the inherent instability of RNA imposes stringent environmental constraints on where and how such life could have persisted 54 , 56 . These limits arise from RNA's chemical vulnerabilities, including susceptibility to hydrolysis, photodegradation, and metal-ion-mediated cleavage, which would have confined viable niches to protected microenvironments capable of mitigating these stressors. Central to these constraints is RNA's lability in aqueous environments, often termed the "water paradox" in prebiotic chemistry: water is essential for biomolecular interactions yet promotes backbone hydrolysis via the 2’-OH group, with half-lives ranging from hours to days under neutral pH and ambient temperatures. Elevated temperatures exacerbate this, as RNA unfolding and degradation accelerate above ~ 60–80°C, rendering high temperature hydrothermal settings improbable for sustained RNA replication despite their potential for organic synthesis 56 . Furthermore, Hadean atmospheric greenhouse forcing after large impacts plausibly warmed the surface 30 . It is also hypothesized that variable production of reduced gases such as H 2 and CH 4 along with residual heat pulses from late accretion impacts further prolonged warm to hot surface conditions throughout the Hadean 29 , 31 . If surface temperatures were high (50–70°) at that formative time 20 , only cooler refugia - such as subsurface aquifers or polar regions - would have offered thermal stability to RNA organisms. Moreover, stochastic short-lived environmental fluctuations, including periodic local high-temperature spikes from local impacts or regional volcanism, could disrupt RNA oligomer concentrations by 20–40%, as modeled in resource-constrained simulations of prebiotic systems 57 . Ultraviolet (UV) radiation from the young Sun, intensified by both the activity of our star in its youth and the lack of an effective ozone layer in the early atmosphere, presents another formidable barrier, causing photodamage to nucleobases and strand breaks 58 . Solar UV fluxes were estimated to be 10–100 times higher in the Hadean than today, sufficient to degrade exposed RNA within minutes to hours, necessitating shielding mechanisms like simple pigment-like structures, mineral adsorption, submersion in turbid waters 59 . Both pH extremes further limit RNA viability: acidic conditions (pH 10) may favor nucleotide synthesis but risk deamination; thus, mildly alkaline hydrothermal systems (pH 8–10) emerge as plausible crucibles for the RNA World, as they could facilitate RNA polymerization on minerals or rock glasses to stabilize oligomers against dilution and degradation 60 , 61 . Metal ions, abundant in Hadean oceans from crustal leaching and impact delivery, further add to this complexity: divalent cations like Mg 2+ are required for ribozyme folding and catalysis but can also promote phosphodiester cleavage at concentrations above ~ 10 mM 62 . This dual role of Mg 2+ suggests that low-metal environments, perhaps in freshwater ponds hosted by emergent land as previously inferred from zircon oxygen isotopic data 37 , would have been more conducive to starting off an RNA World. Such environments allow for wet-dry cycles that concentrate reactants without excessive ion interference. Salinity poses additional challenges, as high ionic strength disrupts RNA secondary structures, favoring dilute or brackish settings over hypersaline basins. Debates persist regarding optimal locales, with submarine hydrothermal vents offering geochemical energy and mineral catalysis but risking thermal and pH instabilities 63 , as well as dilution of prebiotically useful components. This contrasts with warm springs or evaporative ponds on land surfaces that enable cyclic dehydration for polymerization 46 and favor concentration. Recent models highlight fluctuating conditions that mirror Hadean impact-driven perturbations: these impose temporal limits, with RNA persistence reliant on episodic stabilization rather than continuous equilibrium 57 . Such environmental boundaries shaped not only the distribution of RNA life but also the selective pressures that determined its functional capabilities, as discussed in the following section on metabolic styles. Hadean metabolic styles The environmental constraints delineated for RNA organisms, coupled with their rudimentary nature as self-replicating ribozyme systems, imply that their metabolic capabilities were inherently limited and intimately tied to the geochemical disequilibria of the Hadean Earth. In the RNA World framework, metabolism would have been orchestrated by ribozymes catalyzing essential reactions for self-maintenance and replication, drawing on prebiotic organic pools or in situ synthesis to sustain nucleotide monomers and energy equivalents 7 , 64 . These proto-metabolic styles likely spanned a continuum from pseudo-heterotrophic exploitation of exogenous organics - delivered via impacts or atmospheric photochemistry - to nascent autotrophic pathways leveraging hydrothermal redox gradients, with cooperative networks emerging to overcome individual catalytic inefficiencies 39 , 65 . Besides the proposed concept of protocells absorbing prebiotically produced monomers, another scenario could include the absorption of prebiotic compounds such as formamide, cyanamide, or glycolaldehyde by the protocells from the environment, with ribozymes facilitating their condensation into nucleotides or energy-rich intermediates 66 . For instance, non-enzymatic reactions amplified by RNA catalysis mimic aspects of the formose reaction, generating sugars like ribose under fluctuating wet-dry conditions in ponds on land, thereby fueling oligomer assembly without complex enzymatic cascades. These processes would predate the appearance of carbon fixation from CO 2 . This opportunistic style aligns with the dilute, variable Hadean surface environments, where RNA's catalytic promiscuity - enabling a single ribozyme to perform multiple reactions - compensated for low substrate specificity and turnover rates 56 . Such dependence, however, on external organics by pseudo-heterotrophy would have been vulnerable to depletion. This tension ultimately favors selection for more self-sufficient systems. Autotrophic inclinations, particularly in alkaline hydrothermal vents, represent a complementary style wherein RNA organisms may have harnessed geochemical energy for carbon fixation and reduction 63 . Primitive versions of the Wood–Ljungdahl pathway, driven by H 2 and CO 2 across mineral membranes, could have been ribozyme-assisted to produce acetyl thioesters as primitive energy currencies akin to acetyl-CoA 3 . In this scenario, metal cofactors (e.g., Fe-S clusters, or transition metals, like nickel and cobalt) are integrated with ribozymes to catalyze reductive carboxylation, bridging geochemistry to biochemistry in what has been termed a "semi-enzymatic" network 65 . Similarly, segments of the reverse tricarboxylic acid cycle might have operated abiotically with RNA enhancing efficiency, generating organic acids like pyruvate for nucleotide precursors under mild alkaline, reducing conditions. Such deep ancient pathways, rooted in Hadean vent chemistry modulated by what we can tell about the nature of the earliest crust, reinforces that concept of a metabolism-replication coupling where RNA replicators collectively sustained monomer pools, as modeled in surface-bound or vesicular communities 67 . Cooperative dynamics further characterized RNA metabolic styles, with replicator ensembles forming hypercycles or compartmentalized groups to ensure complete catalytic coverage 67 , 68 . On mineral surfaces, spatial structuring mitigated replicators, allowing metabolic completeness through group selection, while proto-cellular encapsulation intensified this by linking replication to shared metabolism. Such networks, potentially incorporating peptides (short proteins) for enhanced catalysis and stabilization, laid the groundwork for evolutionary refinement without preempting the genetic takeover by DNA. The road to LUCA ran through an RNP World Unlike the classical RNA World hypothesis, which posits a stage dominated solely by catalytic RNA molecules, the RNP World emphasizes the subsequent or concomitant coevolution and integration of RNA with peptides and proteins into functional ribonucleoprotein assemblies 15 , 69 – 70 . The RNP World was therefore an intermediate stage where RNA catalysis and primitive peptide synthesis formed a system with greater catalytic versatility, structural stability, and evolutionary potential than either RNA or peptide alone. The central tenet is that RNPs emerged when RNA molecules and short peptides began to create organized, reproducible interactions that conferred catalytic robustness and information transfer advantages relative to RNA. This coevolutionary framework appears to overcome critical limitations of the RNA World model, particularly the chemical instability of RNA under prebiotic conditions particular to the Hadean Earth, and the limited catalytic repertoire of ribozymes compared to protein enzymes. At the molecular level, the RNP World is characterized by several key features which differentiate it from the hard RNA World. First, the Peptidyl Transferase Center (PTC) of the ribosome and proto-tRNA concatenation systems are proposed as early organizing structures that could bootstrap coded peptide formation and establish a primitive translation apparatus 15 , 69 . These proto-ribosomal assemblies may have provided a platform for the evolution of the genetic code and the gradual refinement of translation fidelity. Second, ribosomal RNAs and proteins appear to have undergone incremental accretion and coevolution, with small subunit processivity features predating the PTC catalytic core, implying a gradualist build-up of modern ribosomes from simpler RNP ancestors 70 . Interestingly, this structural phylogenetic evidence suggests that the ribosome itself is a molecular fossil preserving the evolutionary history of the RNP World. Like RNA organisms, RNP organisms likely also possessed short, structured RNA genomes that functioned both as genetic material and catalysts, with heritable replication mediated by ribozymes or peptide-assisted RNA polymerases 70 , 71 . The inherent chemical instability of ribonucleotides under physiological conditions would have favored short RNA molecules with extensive secondary and tertiary structure, which could be stabilized through association with cationic or hydrophobic peptides 72 , 73 . Proto-tRNAs and tRNA concatenates are hypothesized to have served dual roles as adaptors for primitive peptide synthesis and as modular building blocks for early genes 15 , 69 . This tRNA-centric model of genetic organization suggests that the operational RNA code - the assignment of amino acids to specific RNA structures - preceded and scaffolded the emergence of the triplet genetic code. The catalytic machinery of RNP organisms were built around ribozyme cores performing essential functions such as RNA replication, peptide bond formation, and RNA processing 72 . Ancient ribozymes like RNase P RNA and PTC-like motifs provided key catalytic activities 74 , while associated proteins or short peptides progressively improved catalytic efficiency and substrate recognition 72 . Experimental evidence demonstrates that short cationic and hydrophobic peptides can adsorb onto RNA, stabilize secondary structures, and enhance the catalytic rates of polymerase ribozymes and other catalytic RNAs 70 , 73 . We posit that these wild environmental peptide-RNA interactions became more efficient over time through a positive feedback loop: RNA-encoded peptides enhance RNA catalysis, which in turn enables more efficient peptide synthesis and the evolution of longer, more complex proteins. Non-canonical nucleoside chemistry provides additional support for RNA-peptide coevolution. Experiments have shown that peptide synthesis can occur directly on RNA scaffolds through non-canonical nucleoside linkages, producing peptide-RNA chimeras that demonstrate plausible prebiotic routes to integrated RNA-peptide systems and proto-translation chemistry 70 . Such chimeric molecules may have been the first entities capable of both information storage and catalytic function, bridging the gap between simple self-replicating molecules and modern cells, between RNA/RNP and the DNA/LUCA. The functional units of RNP organisms were likely ribonucleopeptide complexes and proto-ribosomal assemblies that combined RNA scaffolds with small proteins or peptides into integrated catalytic factories 70 . These RNP complexes would have operated within membrane-bound cells either free living or attached to mineral surface microenvironments, which concentrated reactants and protected fragile RNA molecules from degradation. The population structure of early RNP organisms may have been communal rather than clonal, with ensembles of diverse RNA sequences and peptide libraries creating an innovation-rich milieu characterized by frequent horizontal gene transfer and recombination. This genetic promiscuity accelerated evolutionary innovation by allowing beneficial mutations and molecular inventions to spread rapidly through the population. The transition from RNP-based organisms to modern DNA-protein cells involved multiple interconnected processes: the emergence of sophisticated protein catalysts, the invention of DNA as a stable genetic storage medium, and the refinement of the translation system to its modern form. The evolution of complex proteins from simple peptides proceeded through a feedback cycle in which improving translation allowed RNA-encoded peptides to fold into more effective RNA-binding and enzymatic proteins, which in turn enabled more efficient replication and expansion of genetic information. This positive feedback would have driven the gradual replacement of ribozyme catalysts by protein enzymes, as proteins offered superior catalytic versatility, specificity, and evolvability. Ancestral protein folds could have arisen from short peptides initially selected for RNA-binding and structural support, which subsequently acquired enzymatic functions through gene duplication and divergence 73 . The ribosome itself underwent a complex evolutionary trajectory from primitive PTC/tRNA systems to the multi-subunit molecular machine found in modern cells 70 . Structural and phylogenetic analyses reveal that small subunit components linked to mRNA binding and translational processivity likely evolved before the large subunit catalytic center, facilitating improvements in translation fidelity and the expansion of the genetic code 70 . The accretion model of ribosomal evolution, supported by comparative structural phylogenetics, suggests that ribosomal RNA and protein components were added incrementally, with each addition conferring selective advantages in translation speed, accuracy, or regulatory capacity. Theoretical analyses that integrate biochemical plausibility, structural data, and evolutionary logic increasingly favor an early RNA-protein (RNP) stage as more feasible than a pure RNA World leading directly to a DNA World. Models of genetic code origin that link proto-tRNAs, PTC formation, and the operational/anticodon code provide mechanistic pathways for the emergence of coded translation within an RNP framework 15 , 69 . These models demonstrate that the key innovations of molecular biology - replication, transcription, and translation- emerged through the coevolution of RNA and peptide components, rather than requiring a purely RNA-based precursor stage. Dawn of the DNA World The metabolic adaptations of RNA organisms to RNP organisms, as constrained by Hadean geochemistry and reliant on ribozyme networks, likely persisted for a relatively geologically brief (ca. 150 Myr) interval before yielding to DNA-based heredity. This is most strongly evidenced by the phylogenetic placement of LUCA. Integrating molecular clock analyses with geochronological data, these studies constrain the RNA and RNP Worlds’ duration to approximately 100–200 million years 2 , 4 . This compressed timeline reconciles rapid prebiotic assembly in post-impact reducing atmospheres 29 facilitating nucleotide synthesis via HCN and nitriles with the swift evolutionary ascent to LUCA's complexity which encompasses a ~ 2.5 Mb genome encoding ~ 2,600 proteins 2 , 3 . The RNA World (primordial) relied on self-replicating RNA for both information and catalysis, the RNP World featured RNA acting with proteins for enhanced function, and the DNA World utilizes stable, double-stranded DNA for storage with protein enzymes for metabolism (Fig. 5 ). As previously mentioned, divergence time estimates, calibrated against microbial fossils and gene duplications predating LUCA, consistently position this ancestor in the late Hadean, with a median age of 4.2 Gyr and ranges extending from 3.94 to 4.52 Gyr. This is an important datum in our argument because the RNA-to-DNA handover would have occurred amid ongoing late accretion, where impact-driven perturbations accelerated selection for more stable genetic systems without necessitating protracted stasis. Evidence from ancestral gene reconstructions further supports this rapidity: the innovation of ribonucleotide reductases and thymidylate synthases - enabling deoxyribonucleotide production from RNA precursors - likely arose within this 100–200 Myr window, potentially via ribozyme-to-protein catalysis shifts 75 . Stepwise models propose a three-phase progression from autocatalytic RNA networks to template-directed replication, aligning with the swift integration of DNA for enhanced fidelity 65 , 76 . Biogeodynamic contextualization reinforces this brevity: with emergent land and hydrological cycles fostering diverse niches, RNA populations could diversify rapidly, but Hadean environmental stresses – UV fluxes, thermal excursions and ion imbalances – would impose stringent limits on scalability, favoring the genetic transition. This temporal framework, while not precluding lingering RNA entities in refugia, demarcates the RNA World's eclipse as a pivotal threshold, driven by environmental pressures that ultimately favored DNA-centric life. Why DNA prevailed over RNA and RNP The circumscribed duration of the RNA World, as inferred from phylogenetic and geodynamic evidence, stresses the evolutionary imperatives that propelled the ascendancy of DNA as the principal genetic material. We have reviewed how RNA's versatility enabled the inception of replication and metabolism, but its intrinsic limitations - chemical instability, propensity for misfolding, and error-prone replication - rendered it ill-suited for sustaining increasingly complex biospheres, paving the way for DNA's selective dominance 54 , 55 . We propose that this was not abrupt but emerged through incremental biochemical innovations exploiting DNA's more fit and robust attributes that were driven by the Hadean environmental pressures favoring enhanced genomic reliability and scalability. RNA has inferior chemical and structural stability The lack of 2'-hydroxyl group is a disadvantage to RNA. Whereas DNA contains deoxyribose, the 2'-OH group is still present in RNA's ribose sugar. This -OH group makes RNA highly susceptible to hydrolysis and rapid degradation. DNA’s backbone is far less prone to cleavage, making it a more robust repository for genetic data. As a double helix, the structure of DNA protects the nitrogenous bases inside the structure. This configuration shields information from chemical damage (e.g., UV light, hydrolysis). Uracil is used in RNA and because DNA instead uses thymine (5-methyluracil), it provides additional stability and is more resistant to photochemical mutations compared to uracil. Temperatures above about 50 ˚C, and pH > 8 are detrimental to RNA structures. These are also unstable at seawater salinities. RNA has lower replication fidelity and repairability DNA replication is far less error-prone than RNA replication, allowing for the stable transmission of much larger genomes. This is because the complementary double-stranded structure allows for error-checking and repair. If one strand is damaged, the other can serve as a template for repair. Cytosine often breaks down into uracil (deamination). In DNA, the presence of uracil can be easily identified as foreign and repaired. In an RNA world, uracil is a natural base, making such repairs impossible 78 . RNA is unable to support larger genomes Since DNA is less likely to self-fold into complex 3D structures (a common issue for RNA), it is more suitable as a template. This allows DNA to form long, linear, or circular structures (chromosomes) that can store vast amounts of information without getting tangled or degraded. Due to its stability, DNA can act as a long-term, passive hard drive for genetic information, while RNA is better suited for short-term, active roles in protein synthesis. The RNP World is a short-lived compromise Several key advantages exist for the transitional RNP World over the classic RNA World to DNA World scenario, primarily by addressing the inherent instability of pure RNA and its limited catalytic repertoire. The RNP World posits that early biological systems formed a partnership between RNA and peptides, allowing them to overcome the limitations of relying on RNA alone. Such a partnership increased stability by protecting RNA from degradation. As RNA is notoriously chemically unstable and prone to hydrolysis the binding of proteins (or peptides) to RNA in RNP complexes shielded RNA from degradation. Peptides can provide structural stability to RNA molecules, allowing them to form complex, durable shapes that would be impossible for single-stranded RNA on its own 70 . While RNA can act as a catalyst (ribozyme), its repertoire is limited compared to protein enzymes. Peptides introduce a wider range of chemical properties (hydrophobic and hydrophilic) that enhance the catalytic rate of reactions. Compared to RNA alone, RNP complexes combine the best of both worlds: the information storage of RNA and the efficient catalysis of proteins. The RNP transition also solves the dilemma of which came first -functional proteins or informational RNA - by proposing they co-evolved as partners from the earliest stages. Amino acids (the building blocks of proteins) were available in early Earth conditions and could have served as cofactors, enabling faster synthesis of RNA-related molecules compared to an RNA-only environment. The RNP World is supported by modern biology, as the ribosome (which synthesizes all proteins) is itself a complex ribonucleoprotein, with RNA acting as the catalyst. It provides a more realistic, gradual pathway from simple prebiotic chemistry to the complex, DNA-based life we know today, rather than requiring a sudden, improbable jump to a fully functional RNA-only system. Bottlenecks Foremost among DNA's advantages is its heightened chemical stability, stemming from the absence of the 2'-hydroxyl group on deoxyribose 78 . In contrast to RNA's labile single-stranded forms, DNA's canonical double-helix structure further bolsters durability, enabling the archiving of longer sequences with reduced degradation rates – essential for accommodating the ~ 2.5 Mb genome inferred for LUCA 2 . Computational analyses reveal that DNA strands exhibit folding free energies approximately tenfold higher than RNA counterparts, minimizing secondary structures that impede template accessibility and replication fidelity. This stability facilitated the separation of informational roles, with DNA serving as a robust repository while RNA retained catalytic and intermediary functions, alleviating the dual burden on RNA in primordial systems. Mechanistic pathways for this shift likely involved the prebiotic or early biotic synthesis of deoxyribonucleotides from ribonucleotide precursors, catalyzed by proto-enzymes or ribozymes akin to modern ribonucleotide reductases 75 . Non-enzymatic templating of DNA strands on RNA scaffolds, followed by enzymatic replication via emergent RNA-dependent DNA polymerases or reverse transcriptase-like activities, would have initiated chimeric RNA-DNA systems. The incorporation of thymine over uracil further enhanced error detection. In silico simulations and experimental models demonstrate that such genetic takeovers could occur under fluctuating conditions, with DNA-enriched protocells outcompeting RNA-only variants through superior heritability and reduced mutational load 15 . These general advantages created the first bottleneck effect – where RNA organisms drastically fell behind DNA organisms in the competition, creating a decline in their numbers, allowing DNA based life to flourish. Selective forces in Hadean milieux – ion imbalances, thermal cycles, and impact-induced disruptions – amplified these benefits, as populations with DNA-mediated heredity exhibited greater resilience and adaptive potential, culminating in the DNA-protein World's establishment by LUCA. This creates the second bottleneck, driven by the environmental factors. This evolutionary pivot not only resolved the RNA World's vulnerabilities but also enabled the diversification that defines contemporary life. The transition from RNA to DNA genomes remains one of the most enigmatic events in early evolution. Several scenarios have been proposed to explain this shift. One prominent hypothesis invokes viral or retroelement-mediated introduction of reverse transcription and ribonucleotide reductase activities, which would have enabled the synthesis of DNA nucleotides and the copying of RNA genomes into more stable DNA forms. Alternative models suggest independent inventions of DNA synthesis in separate lineages, driven by selection for more stable genetic storage in increasingly complex organisms 78 . Importantly, the transitions to DNA-based genomes and fully proteinaceous enzyme systems need not have occurred synchronously across all lineages. Evidence supports parallel or independent transitions in different lineages descended from communal RNP progenitors, with some lineages adopting DNA earlier than others 78 . This mosaic pattern of evolutionary innovation is consistent with the progenote concept, which views early life as a diverse community of organisms with partially formed, error-prone genetic and translational systems that gradually refined through natural selection and horizontal gene transfer. The relationship between the RNP World and the Last Universal Common Ancestor (LUCA) is central to understanding the deep evolutionary history of life. Rather than viewing LUCA as a single cell with modern biochemistry, recent analyses frame LUCA as a descendant of RNP-era populations, possibly representing a complex, genetically redundant community shaped by its RNP legacy. Several lines of evidence suggest that LUCA may have been a complex, possibly mesophilic community with extensive genetic redundancy and traces of RNA-based heredity consistent with RNP ancestry 78 . This community model resolves several paradoxes in LUCA reconstruction, including the presence of apparently incompatible biochemical features and the difficulty of reconciling LUCA’s inferred complexity with the simplicity expected of early life. We argue that LUCA was a community rather than a single organism, which means horizontal gene transfer among community members would have homogenized many genes while allowing lineage-specific innovations to persist in different subpopulations. Discussion The RNA World hypothesis, which elevates RNA to being the primordial genetic and catalytic material, provides a framework for life's inception amid the Hadean Earth's geodynamic environment. Life's emergence coincided with the rapid assembly of RNA replicators in clement niches on Hadean Earth. These niches were circumscribed by late accretion bombardment and modulated by early hydrological cycles that supplied organics and energy gradients 4 , 37 . The RNA organisms were minimalist, autonomous protocells distinct from modern viruses that navigated stringent environmental limits. These included the water paradox, UV fluxes, and ionic perturbations, confining them to protected hydrothermal or terrestrial settings where ribozyme catalysis enabled heterotrophic scavenging or nascent autotrophy 55 , 63 , 65 . Metabolic styles, from opportunistic formose-like reactions to proto-Wood–Ljungdahl pathways in cooperative networks, underscored RNA's versatility but also its fragility, with low fidelity and instability constraining scalability 3 , 67 . The RNP World hypothesis provides a coherent and mechanistically plausible waystation from the RNA World to DNA genomes and the emergence of LUCA. By emphasizing the coevolution of RNA and peptides into integrated functional systems, the RNP World model addresses key limitations of the pure RNA World hypothesis and offers testable predictions about the molecular organization, catalytic capabilities, and evolutionary trajectories of early organisms. The ribosome, as a molecular fossil preserving the architecture of ancient RNP assemblies, stands as a testament to this deep evolutionary history. This brevity of the RNA and RNP Worlds - spanning 100–200 Myr before LUCA's advent at ~ 4.2 Gyr ago – is dictated by the intense environmental pressures of the Hadean Earth’s surface, where late accretion impacts and geochemical fluctuations selected for DNA's superior stability, fidelity, and informational capacity. The transition to DNA, mediated by ribonucleotide reduction and chimeric templating, resolved RNA's vulnerabilities, enabling the DNA-protein paradigm that underpinned LUCA's genomic sophistication and the biosphere's persistence 15 . Our analysis does not in any way diminish the RNA World's foundational role but frames its demise as an evolutionary imperative: Without the handover to DNA, life's trajectory toward complexity might have stalled, as recent ribozyme reconstructions affirm RNA's catalytic prowess yet highlight its inadequacy for long-term evolvability in dynamic environments. Original insights from this synthesis suggest that the RNA and RNP Worlds’ fall was not merely a biochemical improvement but a biogeodynamic upgrade that potentially happens on exoplanets with similar accretionary histories. For instance, if Hadean-like impacts accelerated nucleotide synthesis and selection, then biocompatible worlds with clement surfaces around young Sun-like (F,G,K) stars might also be expected to host at least fleeting RNA phases. Conversely, this transience challenges the orthodox "Hard RNA World” variant, by implying a continuum where peptides and DNA co-emerged earlier than presumed, as evidenced by studies on RNA-sulfur interactions fostering proto-peptides 66 . Future research should refine models integrating these findings, perhaps through in vitro experiments with protocells enclosing RNA strands that are exposed to RNA monomers in solution to test the pseudo-heterotrophy concept. Ultimately, the RNA World's swift eclipse illuminates the resilience of early life rather than its fragility, transforming a hypothesized precursor into life’s first actor in Earth's biogeodynamic narrative. Materials and Methods Figure 3 , shows the instantaneous percent of lithosphere molten over time, was generated using a three-dimensional impact bombardment model of the Hadean Earth’s lithosphere 31 , 33 , 34 . A stochastic cratering model populated the surface with craters according to the Brasser late accretion chronology 28 , delivering a total mass of 0.57 wt% Earth (≈ 3.4 × 10 22 kg) between 4.5 and 3.5 Ga, with a size-frequency distribution of rocky impactors 31 analogous to the main asteroid belt and impact velocity distribution derived from dynamical simulations 31 . Simulations were initiated from either a pre-existing crust (baseline) or a global magma ocean formed by the Moon-forming impact 27 . Basaltic target properties were adopted (surface temperature 20°C, geothermal gradient 70°C km − 1 , density 3000 kg m − 3 , heat capacity 800 J kg − 1 °C − 1 , thermal conductivity 2.5 W m − 1 °C − 1 , solidus 1100°C). Melting was defined as crustal material being heated above the basalt liquidus temperature of ~ 1250°C, while accounting for the latent heat of fusion of basalt at ~ 400 kJ kg − 1 in the energy balance. At each time step the model computed the volume of lithosphere exceeding the criteria for melting and expressed this as a percentage of the total lithosphere volume, yielding the instantaneous molten fraction for the two initial states. The data to reproduce Fig. 3 is provided in Supplementary data file Fig. 3 _data.xls. Declarations Acknowledgments Funding: This work was supported by the ERC Horizon Europe funding programme in support of the Synergy Grant - GEOASTRONOMY, grant agreement number 101166936 (to S.J.M.. O.A.), funding from the Research Center for Astronomy and Earth Sciences (CSFK), an MTA Center of Excellence, in Budapest, Hungary (to A.M., O.A. and S.J.M.) and the Institute of Paleobiology Polish Academy of Sciences (to B.K.). The idea for this paper was an outcome of the Biogeodynamics COST Action CA23150 “EUROBiG”, supported by the European Cooperation in Science and Technology. Author contributions: Conceptualization: A.M., S.J.M., B.K., and O.A. Methodology: A.M., S.J.M.. Software: O.A. Data curation: O.A.. Formal analysis: A.M., S.J.M. Investigation: A.M., B.K.. Validation: A.M., B.K., S.J.M.. Visualization: S.J.M.. and O.A.. Writing—original draft: A.M., S.J.M., O.A. and B.K.. Writing—review and editing: A.M., O.A., B.K. and S.J.M.. Resources: S.J.M.. Funding acquisition: S.J.M.. Project administration: S.J.M.. Supervision: S.J.M. and B.K. Competing interests: The authors declare that they have no competing interests. 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Part A: Emergence of the hypercycle. Naturwissenschaften 64 , 541–565 (1978). https://doi.org/10.1007/BF00450633 Saad, N. Y. A ribonucleopeptide world at the origin of life. J. Syst. Evol. 56 , 1–13 (2018). https://doi.org/10.1111/JSE.12287 de Farias, S. T. & Prosdocimi, F. RNP-world: The ultimate essence of life is a ribonucleoprotein process. Genet. Mol. Biol. 45 , e20220127 (2022). https://doi.org/10.1590/1678-4685-GMB-2022-0127 Landweber, L. F. Testing ancient RNA-protein interactions. Proc. Natl Acad. Sci. USA 96 , 11067–11068 (1999). https://doi.org/10.1073/pnas.96.20.11067 Cech, T. R., Moras, D. & Nagai, K. The RNP World. In The RNA World 3rd edn (eds Gesteland, R. F., Cech, T. R. & Atkins, J. F.) 309–335 (Cold Spring Harbor Laboratory Press, 2006). https://doi.org/10.1101/087969739.43.309 de Farias, S. T., do Rêgo, T. G. & José, M. V. tRNA core hypothesis for the transition from the RNA World to the Ribonucleoprotein World. Life 6 , 15 (2016). https://doi.org/10.3390/LIFE6020015 Di Giulio, M. The RNase P, LUCA, the ancestors of the life domains, the progenote, and the tree of life. Biosystems 212 , 104604 (2022). https://doi.org/10.1016/j.biosystems.2021.104604 Freeland, S. J., Knight, R. D. & Landweber, L. F. Do proteins predate DNA? Science 286 , 690–692 (1999). https://doi.org/10.1126/science.286.5440.690 Szostak, J. W. The narrow road to the RNA world. Nat. Rev. Mol. Cell Biol. 26 , 345–347 (2025). https://doi.org/10.1038/s41580-025-00721-4 Vértessy, B. G. & Tóth, J. Keeping uracil out of DNA: Physiological role, structure and catalytic mechanism of dUTPases. Acc. Chem. Res. 42 , 97–106 (2009). https://doi.org/10.1021/ar800114w Altstein, A. D. The progene hypothesis: The nucleoprotein world and how life began. Biol. Direct 10 , 67 (2015). https://doi.org/10.1186/S13062-015-0096-Z Additional Declarations No competing interests reported. Supplementary Files Fig3data.xlsx Cite Share Download PDF Status: Under Revision Version 1 posted Editorial decision: Revision requested 14 May, 2026 Reviews received at journal 13 May, 2026 Reviews received at journal 28 Apr, 2026 Reviewers agreed at journal 17 Apr, 2026 Reviewers agreed at journal 17 Apr, 2026 Reviewers invited by journal 16 Apr, 2026 Editor assigned by journal 15 Apr, 2026 Editor invited by journal 15 Apr, 2026 Submission checks completed at journal 10 Apr, 2026 First submitted to journal 10 Apr, 2026 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-9212823","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":625099514,"identity":"45cae14d-4ad2-436d-89a6-a690dcf0131b","order_by":0,"name":"Anna Medvegy","email":"","orcid":"","institution":"Eötvös Loránd University","correspondingAuthor":false,"prefix":"","firstName":"Anna","middleName":"","lastName":"Medvegy","suffix":""},{"id":625099515,"identity":"66e569da-5876-4f67-b0e5-7f724c956593","order_by":1,"name":"Oleg Abramov","email":"","orcid":"","institution":"University of Bayreuth","correspondingAuthor":false,"prefix":"","firstName":"Oleg","middleName":"","lastName":"Abramov","suffix":""},{"id":625099516,"identity":"6e1c169c-ab9d-47b9-bfdc-c685c0134cf5","order_by":2,"name":"Barbara Kremer","email":"","orcid":"","institution":"Polish Academy of Sciences","correspondingAuthor":false,"prefix":"","firstName":"Barbara","middleName":"","lastName":"Kremer","suffix":""},{"id":625099517,"identity":"594060b7-9f82-4427-8e7d-74f1e58e4cfa","order_by":3,"name":"Stephen Mojzsis","email":"data:image/png;base64,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","orcid":"","institution":"University of Bayreuth","correspondingAuthor":true,"prefix":"","firstName":"Stephen","middleName":"","lastName":"Mojzsis","suffix":""}],"badges":[],"createdAt":"2026-03-24 13:53:27","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-9212823/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-9212823/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":107869325,"identity":"56ca039c-4930-4d38-879f-0608eebd5921","added_by":"auto","created_at":"2026-04-27 07:36:44","extension":"jpg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":104607,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eBiogeodynamic timeline of Earth history\u003c/strong\u003e (time units are in 10\u003csup\u003e9\u003c/sup\u003e years expressed in log\u003csub\u003e10\u003c/sub\u003e scale). Here are shown events in geologic history correlated with a simplified representation of the divergence of lineages from the LUCA organisms (modified after\u003csup\u003e2\u003c/sup\u003e). Predating the LUCA are earlier steps from the unclear origins of prebiotic chemistry to the more tangible RNA and RNP worlds. The concept of a “pseudo-heterotrophy” shown here as the first metabolic style visualizes early life forms and/or RNA based structures that relied on incorporating prebiotically produced organic molecules from the environment for growth and function. Prot = Proterozoic eon (2.5-0.542 Gyr ago); Ph = Phanerozoic eon (0.542-0 Gyr ago). LACA = Last Archaea Common Ancestor; LBCA = Last Bacteria Common Ancestor; Ar = Archaea; Eu = Eukarya; Ba = Bacteria.\u003c/p\u003e","description":"","filename":"Figure1Medvegy2026.jpg","url":"https://assets-eu.researchsquare.com/files/rs-9212823/v1/669fcb2d67004d0ad77a6c44.jpg"},{"id":107769037,"identity":"2757ae8b-3ded-4955-bc76-a282e9fae0a6","added_by":"auto","created_at":"2026-04-25 03:27:01","extension":"jpg","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":125321,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eEarth’s oldest direct geological records.\u003c/strong\u003e Shown here are data for the oldest zircon ages expressed in millions of years (Ma) against the number of zircons yielding a particular age (count). The cyan data field are from the Jack Hills outcrop in Western Australia (WA)\u003csup\u003e25\u003c/sup\u003e. Superposed on those data are results from another Hadean zircon locality identified in the Green Sandstone Bed (GSB) in the Barberton Greenstone Belt of South Africa (SA). Note the scale difference for the two data sets (GSB data courtesy of N. Drabon).\u003c/p\u003e","description":"","filename":"Figure2Medvegy2026.jpg","url":"https://assets-eu.researchsquare.com/files/rs-9212823/v1/a8671b2cee2e762951da2066.jpg"},{"id":107869324,"identity":"add6e118-d894-42a1-b242-f71e1786a6fb","added_by":"auto","created_at":"2026-04-27 07:36:44","extension":"jpg","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":91983,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eMelting and cooling from impacts. \u003c/strong\u003eLate accretion-derived instantaneous melt production estimates for Earth’s crust over the course of the Hadean eon, based on models of early solar system impact bombardment\u003csup\u003e31\u003c/sup\u003e.\u003c/p\u003e","description":"","filename":"Figure3Medvegy2026.jpg","url":"https://assets-eu.researchsquare.com/files/rs-9212823/v1/71cf623c43be4333f9bb7e89.jpg"},{"id":107769039,"identity":"185c05e0-b513-43b9-b9de-4922af21a281","added_by":"auto","created_at":"2026-04-25 03:27:01","extension":"jpg","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":112806,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eA schematic representation for the development of the RNA to RNP to DNA Worlds. \u003c/strong\u003eT. Gánti (1997) referred to the most rudimentary unit of life as a chemical automaton (chemoton)\u003csup\u003e6\u003c/sup\u003e. As we present it here, this chemoton-like structure shows encapsulation by lipid or phospholipid bilayers, information from RNA capable of replication, and a proto-metabolic system that emerged out of the pre-RNA World (1). The RNA world example shows the involvement of informational RNA molecules (2) that encode the synthesis of modestly functional RNAs (3). Here, we propose that abiotic nucleic acids and peptides synthesized in the environment pass through the protocell and provide the building blocks for simple self-catalyzed replication (4) and enhance stability of the complexly folded 3D RNA structure (5), respectively. As described in the text, we term this quasi-metabolic process \u003cem\u003epseudo-heterotrophy\u003c/em\u003e (6) as it does not rely on nutrients from the breakdown of existing biomolecules produced by other organisms but instead uses the products of prebiotic chemistry synthesized in nature. Later, protein translation developed (7) along with the intermediate RNP world (8). Following that stage, protein enzymes produced deoxyribonucleotides via ribonucleotide reduction (9). The advent of deoxyribonucleotides led to the DNA genome and the emergence contemporary genetic system just before the LUCA appeared at ca. 4.2 Gyr ago\u003csup\u003e2\u003c/sup\u003e.\u003c/p\u003e","description":"","filename":"Figure4Medvegy2026.jpg","url":"https://assets-eu.researchsquare.com/files/rs-9212823/v1/2a44d9d304d1de18b633f65b.jpg"},{"id":108181321,"identity":"1247cfa1-f3ea-4580-a5ca-612ee308e0d0","added_by":"auto","created_at":"2026-04-30 08:58:33","extension":"jpg","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":98279,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cstrong\u003eStepping stones from the RNA World to the DNA World\u003c/strong\u003e. By itself, RNA is unfit as the informational molecule of a long term biosphere. Several advantages, however, point to RNA coming before DNA in early life: \u003cu\u003eDual Functionality (Catalysis and Storage)\u003c/u\u003e: Unlike DNA, which primarily stores information, RNA can act as both a genotype (information) and a phenotype (catalyst/function), allowing it to facilitate its own replication. \u003cu\u003eRibozymes\u003c/u\u003e: RNA molecules can form complex 3D shapes to catalyse essential chemical reactions (ribozymes), acting like proteins. \u003cu\u003eSimpler Synthesis\u003c/u\u003e: RNA is considered a simpler molecule, likely forming before the more complex DNA, and possesses the ability to form under prebiotic conditions. \u003cu\u003eEvolutionary Flexibility\u003c/u\u003e: Because RNA can catalyse reactions and store information, it could drive Darwinian evolution independently without needing specialized protein enzymes or DNA. \u003cu\u003eAdaptability\u003c/u\u003e: RNA can undergo conformational changes to respond to environmental stimuli, allowing for rapid evolution and adaptation. These advantages were conferred to the subsequent RNP World.\u003c/p\u003e","description":"","filename":"Figure5Medvegy2026.jpg","url":"https://assets-eu.researchsquare.com/files/rs-9212823/v1/8afd6928774873e71fe5b805.jpg"},{"id":108183775,"identity":"1068c26b-83fd-43d2-9c4a-c3dac708501c","added_by":"auto","created_at":"2026-04-30 09:02:44","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1001355,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-9212823/v1/cba68c12-290d-4117-afa5-afb9a84b7f5b.pdf"},{"id":107769035,"identity":"9aa254a6-945b-427f-9e5b-bc92b355c003","added_by":"auto","created_at":"2026-04-25 03:27:01","extension":"xlsx","order_by":0,"title":"","display":"","copyAsset":false,"role":"supplement","size":58784,"visible":true,"origin":"","legend":"","description":"","filename":"Fig3data.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-9212823/v1/1331f69f3ef7b884811b8249.xlsx"}],"financialInterests":"No competing interests reported.","formattedTitle":"Whence the demise and fall of the RNA World?","fulltext":[{"header":"Introduction","content":"\u003cp\u003eLife on Earth is ancient. The prevailing idea has long been that abiogenesis \u0026ndash; the prebiotic chemical progression from non-living to living biochemistry \u0026ndash; could not have occurred until the early Archean eon by which time Earth\u0026rsquo;s surface stabilized after the cessation of late accretion bombardment and reduction of high internal heat approximately 3.8 Gyr ago\u003csup\u003e\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e\u003c/sup\u003e. Growing evidence, however, suggests that conditions on Earth were suitable for life already in its first few hundred million years, during the preceding Hadean eon (4.5-4.0 Gyr ago). Indeed, molecular phylogenetic analysis points to the common ancestry of DNA-protein-based cellular life and the emergence of the Last Universal Common Ancestor (LUCA) by about 4.2 Gyr ago\u003csup\u003e\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e\u003c/sup\u003e. Analysis also shows that the LUCA was relatively sophisticated; it was part of a microbial population that included an anaerobic acetogen which had by then invented both protein translation and a simple immune system. These features point to a long pre-history for biology on the Hadean Earth\u003csup\u003e\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u003c/sup\u003e. While it remains unquantified how long it took for abiogenesis to occur, the window of opportunity for it to happen continues to narrow (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eIf we accept the argument that life\u0026rsquo;s inception coincides with the onset of the fundamental ancestor-descendent relationship that defines Darwinian evolution\u003csup\u003e\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e\u003c/sup\u003e, then the origin of Darwinism requires the origin of biologically useful information in the form of a functional genetic code\u003csup\u003e\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e\u003c/sup\u003e. This eventuality necessitates the establishment of a molecular genetic lineage allowing for heritable variation of a population to be sorted by natural selection without anticipation. Once this informational threshold is crossed, we take the view that an otherwise proto-biological system can be considered alive when it combines the key properties of information, metabolism and encapsulation together into a functional biont\u003csup\u003e\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e\u003c/sup\u003e. That said, well before the central role of DNA appeared in biology, there likely existed a precursor RNA World\u003csup\u003e\u003cspan additionalcitationids=\"CR8\" citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e\u003c/sup\u003e wherein biologically useful information for life started off with a chiral\u003csup\u003e\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e\u003c/sup\u003e RNA information-storage molecules which could copy themselves by catalyzing their own replication without the need for other RNAs or peptides. First hypothesized by Woese, Crick, and Orgel in the 1960s\u003csup\u003e\u003cspan additionalcitationids=\"CR12\" citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e\u003c/sup\u003e, support for the RNA World was bolstered by the discovery of ribozymes showing catalytic properties\u003csup\u003e\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e,\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e,\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e\u003c/sup\u003e. A proposed intermediate stage in early life, the RNA+peptide (ribonucleoprotein; RNP) world, posits that proteins became the catalysts of life at some time before DNA took a central role\u003csup\u003e\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e\u003c/sup\u003e. Once DNA overthrew the RNP world, then contemporary biochemistry began. While this simple scenario remains a rudimentary theoretical account for what was undoubtedly an astoundingly complex sequence of events, the RNA \u0026loz; RNP \u0026loz; DNA model which includes metabolism and encapsulation at the same time, serves as a useful starting point to guide research in the nature and function of the first biomes and their environment. A crucial aspect hanging this argument together is that RNA is capable of autocatalysis in some cases wherein the product acts as the catalyst of its own reaction\u003csup\u003e\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e\u003c/sup\u003e. The origin of informational and functional RNAs may or may not be different from the origin of encapsulation by proto-cells with some kind of proto-metabolism if these formed together, not in isolation, but as a community. Furthermore, we are reminded of the fact that complete living cells are overall exergonic chemical reaction networks, whereas RNA alone (at least, at present) is a chemical structure with the sole function of making protein\u003csup\u003e\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eThe veracity RNA World hypothesis continues to be a topic of healthy debate\u003csup\u003e\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e\u003c/sup\u003e, and to better understand its potential origin and eventual demise we must consider the global environment in which it arose on the Hadean Earth. Understanding the early geodynamic evolution of Earth frames our view of the RNA World and the factors driving the transition to a DNA World. The fact that the LUCA was an outcome of Hadean biogeodynamic processes compels us to ask: What kind of life was an RNA organism? What Hadean environments did it inhabit? What metabolic styles did it employ? If the RNA World ever existed as an operative biosphere, why then did the RNA-to-RNP-to-DNA World transition happen at all? Could there be extant RNA or RNP organisms in the present DNA biosphere? Are RNA viruses metaphorically part of the RNA World?\u003c/p\u003e \u003cp\u003eA geologically early (ca. 4.3 Gyr ago) time for the events in Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e appears to be at odds with long-standing biological assumptions about the Hadean environment and the tempo of life\u0026rsquo;s origin\u003csup\u003e\u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e19\u003c/span\u003e\u003c/sup\u003e. Here we present a biogeodynamic analysis that reconciles molecular clock phylogenies for the LUCA with Hadean Earth geodynamics to address questions about how the first life forms led to the LUCA. In doing so, we absolve several misperceptions about the survival potential of the emergent biosphere on Hadean Earth.\u003c/p\u003e\n\u003ch3\u003ePlanetary surface conditions for the RNA World\u003c/h3\u003e\n\u003cp\u003eUp to now, attempts to place a time frame on when the origin of life could have occurred were hampered by lack of evidence regarding the nature of the Hadean environment and its ability to host sustained and productive prebiotic chemistry. Developments in the last two decades, however, have radically changed our view of primordial Earth from a dry and unproductive hellscape to one eminently suitable for the kinds of chemistry that could support the origin of the RNA World\u003csup\u003e\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e\u003c/sup\u003e. Evidently, if life arose so early, then its origin also predates the terrestrial rock record that would otherwise provide key clues about its natural environment\u003csup\u003e\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e\u003c/sup\u003e. The oldest rocks on Earth are found in the ca. 3.96\u0026ndash;4.06 Gyr old Acasta Gneiss Complex in Canada. Regrettably, the polyphase metamorphic Acasta rocks reveal little about prevailing surface environmental conditions 4 Gyr ago\u003csup\u003e\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e\u003c/sup\u003e. That is because the granite/granitoid protoliths of these gneisses formed in the mid-crust, not at or near the surface. Owing to a long residence time, the Acasta rocks are now expressed as a complex suite of migmatites interleaved with (older) enclaves of hornblende-plagioclase schists\u003csup\u003e\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e\u003c/sup\u003e. Such rocks do not form anywhere near where biochemistry takes place and hence contain no record relevant to it. Rather, sediments formed in liquid water such as shales and chemical precipitates (e.g. banded iron formations) are the best sources of information about environmental conditions in deep time. At the present, however, there are no agreed-upon Hadean rocks of sedimentary origin on Earth that could potentially yield such information about surface conditions at the time of life\u0026rsquo;s emergence. We must rely on other sources of information.\u003c/p\u003e \u003cp\u003eExtending a direct analysis\u0026thinsp;\u0026gt;\u0026thinsp;4 Gyr into time means that we must turn to information gleaned from tiny (\u0026lt;\u0026thinsp;1 mm) ancient detrital zircon (Zr(SiO4)) crystals as old as 4.4 Gyr found in younger sedimentary rocks from Western Australia and South Africa\u003csup\u003e\u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e23\u003c/span\u003e,\u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e24\u003c/span\u003e\u003c/sup\u003e (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). Aside from isotopic and trace element geochemical data which appear to indicate that Hadean crust interacted with liquid water and that this crust included some inventory of continental affinity, a very few of these oldest zircons also host inclusions of isotopically light carbon that may point to a biosphere at 4.10 Gyr ago\u003csup\u003e\u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e26\u003c/span\u003e\u003c/sup\u003e. Although intrinsic conditions for the origin of life indicated by the oldest zircons \u0026ndash; such as a stable crust and hydrosphere \u0026ndash; appear to be favorable for an early origin, important extrinsic effects unique to the Hadean Earth such as intense late accretion bombardment by comets, leftover planetesimals and asteroids were an important limiting factor. Clearly, conditions on a planet\u0026rsquo;s surface must remain favorable long enough, somewhere, for prebiotic chemistry to develop into self-sustaining biology. Otherwise, without such conditions the system will experience an early failure, potentially thwarting any chance for life to take hold.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e"},{"header":"Results","content":"\u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eExogeneous selection pressures\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eA firm upper temporal limit for the origin of life on Earth is imposed by the giant impact hypothesized to have formed the Moon. This event is proposed to have happened after a planetary object of at least Mars-mass (diameter ca. 6800 km) dubbed \u003cem\u003eTheia\u003c/em\u003e collided with the proto-Earth at ca. 4.51 Gyr ago\u003csup\u003e\u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e27\u003c/span\u003e\u003c/sup\u003e. Moon formation was enough to melt crust and mantle rocks down to several hundred kilometers depth, thus eliminating any chance for survival of a nascent biosphere before that time. Another less well-known boundary condition is provided by the postulated Late Veneer event which may have occurred somewhat later at ca. 4.48 Gyr ago\u003csup\u003e\u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e28\u003c/span\u003e,\u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e29\u003c/span\u003e\u003c/sup\u003e. This strike was less intense but nevertheless devastating as it may have involved a lunar-sized object (termed \u003cem\u003eMoneta\u003c/em\u003e) which delivered the final\u0026thinsp;~\u0026thinsp;0.5\u0026ndash;1% of Earth's mass in inner solar system chondritic material, and as a result enriched the terrestrial mantle in highly siderophile elements such as Ir, Pt and Pd at chondritic relative proportions. The rule of thumb for impacts of such magnitude is that they lead to wholesale crustal melting with associated magma oceans of varying depth depending on the mass of the impactor. During post-impact cooling that follows such colossal events, atmospheric greenhouse forcing plays a critical role in regulating magma ocean lifetimes, which range from ~\u0026thinsp;30 to ~\u0026thinsp;500 Myr depending on volume of magma, redox conditions, and volatile inventories. Under rapid cooling scenarios, a quasi-steady-state global radiative equilibrium state can be reached as early as ~\u0026thinsp;2 Myr post-Moon formation\u003csup\u003e\u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e30\u003c/span\u003e\u003c/sup\u003e. Some models for the timelines of magma ocean cooling show that extended windows for clement surface conditions are feasible if cooling times are relatively rapid, such as that expected for a Late Veneer scale impact (e.g. \u0026le;1000 km diameter). This insight may help reconcile the rapid origin of life with phylogenetic estimates for LUCA. Furthermore, that Hadean zircon data seem to indicate a hydrosphere has been present on Earth since ca. 4.4 Ga, would also imply an atmosphere to maintain pressure to keep water liquid. This interdependence of the timing of the last wholesale crustal melting event and subsequent stabilization of the surface to allow prebiotic chemistry to take place underscores how conditions on the Hadean Earth set the stage for the RNA World's brief tenure.\u003c/p\u003e \u003cp\u003eMoreover, dynamical models of planet formation linked to asteroidal meteorite ages\u003csup\u003e\u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e31\u003c/span\u003e\u003c/sup\u003e and cratering statistics also show that conditions conducive to prebiotic chemistry were in place on Hadean Earth before 4.2 Gyr ago\u003csup\u003e\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e\u003c/sup\u003e. Different thermal models that have been reported for the effects of impact bombardments have their limitations, but all agree that there are no obvious barriers to life on Earth for most of the Hadean eon. Previously, it was assumed that an episode in late accretion termed the late heavy bombardment (LHB) at 3.8\u0026ndash;3.95 Gyr set a maximum temporal limit on the origin of a persistent biosphere\u003csup\u003e\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e\u003c/sup\u003e. It is now understood, however, that linking the lunar cratering record with returned Apollo samples is biased by collection on the lunar near side that was extensively modified by Imbrium basin ejecta\u003csup\u003e\u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e32\u003c/span\u003e\u003c/sup\u003e. Modern models for late accretion of leftover material from planet formation\u003csup\u003e\u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e33\u003c/span\u003e,\u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e34\u003c/span\u003e\u003c/sup\u003e, extended to earlier times (4.5 Gyr), generally show that late accretion may even have supported life\u0026rsquo;s emergence (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e). This new view combining information from the Early Earth geology and estimates of the mass flux of impactors over time including the Late Veneer, is also important to the recent formulation of the so-called Discontinuous Synthesis Model\u003csup\u003e\u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e35\u003c/span\u003e\u003c/sup\u003e. This model argues that oligomeric RNA was actively produced on Hadean Earth\u0026rsquo;s surface thanks to one or more transient reduced (H\u003csub\u003e2\u003c/sub\u003e-rich) atmospheres formed via reaction between metallic iron (Fe\u003csup\u003e0\u003c/sup\u003e) from accreting asteroids or planetesimals with surface water or oxidized mantle, or both\u003csup\u003e\u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e29\u003c/span\u003e\u003c/sup\u003e. These early transient H\u003csub\u003e2\u003c/sub\u003e-rich atmospheres were productive sources of prebiotic chemistry before the impact flux waned in the late-Hadean (ca. 4 Gyr ago), by which time life on Earth was in full swing.\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003eEndogenous selection pressures\u003c/h3\u003e\n\u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eAccording to the geologic record and planetary dynamical models of late accretion, Hadean Earth could begin to host life. Already by that time the planet possessed liquid water, simple organic molecules, and free energy from chemical disequilibria. These, and enough time for relatively quiescent surface conditions to become established, allowed for both productive \u003cem\u003eand\u003c/em\u003e sustained prebiotic chemistry to happen. A further outcome of late accretion's impact flux was to boost supply of exogenous organics and volatiles, such as water, phosphate and carbon compounds to the surface zone to help feed prebiotic chemistry\u003csup\u003e\u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e36\u003c/span\u003e\u003c/sup\u003e. Recent progress in geochronology, isotope geochemistry, and mineral chemistry of the Hadean terrestrial zircons also shows evidence for emergent land and a functioning hydrological cycle by about 4.0 Gyr ago. Specifically, low \u003csup\u003e18\u003c/sup\u003eO/\u003csup\u003e16\u003c/sup\u003eO oxygen isotopic values in detrital zircons collected from the Jack Hills of Western Australia and the Barberton Greenstone Belt in South Africa, attest to interactions between meteoric freshwater and crust that in turn implies the presence of exposed landmasses, rainfall, catchment and weathering processes\u003csup\u003e\u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e37\u003c/span\u003e\u003c/sup\u003e. Taken together, the primordial establishment of a dynamic crust-hydrosphere-atmosphere interface means that environments allowing for prebiotic chemistry, such as wet-dry cycles in shallow ponds or hydrothermal systems on land\u003csup\u003e\u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e38\u003c/span\u003e\u003c/sup\u003e and fed by local prebiotic chemical reactors were present to concentrate reactants and promote the assembly of RNA precursors, protocellular structures and focus accumulation of other environmentally-processed prebiotic molecules.\u003c/p\u003e \u003cp\u003eAlso, zircon trace-element and isotopic data, analyzed via machine learning reconstructions of parental magmas, show that Hadean crust already contained significant felsic components composed of tonalite-trondhjemite-granodiorite suites and potassic granites formed through shallow-depth partial melting at convergent plate margins\u003csup\u003e\u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e39\u003c/span\u003e,\u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e40\u003c/span\u003e\u003c/sup\u003e. The significance of such a geodynamic setting is that it promotes crustal stabilization and volatile recycling, that in turn enhances the availability of disequilibrium chemistry to drive chemical complexity at the global scale\u003csup\u003e\u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e41\u003c/span\u003e\u003c/sup\u003e. This feature of planetary-scale redox linking the transfer of electrons from mantle to crust to hydrosphere to atmosphere is the geochemical basis of what makes Earth a biocompatible planet.\u003c/p\u003e \u003cp\u003eWith the planetary dynamics modeling and the late accretion impact flux estimates cited above, we can begin to parameterize what features the first metabolic styles could have had\u003csup\u003e\u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e42\u003c/span\u003e\u003c/sup\u003e and the relationships of these to the earliest geologic stages of our planet\u0026rsquo;s evolution.\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e\n\u003ch3\u003eThe pre-DNA biome in context\u003c/h3\u003e\n\u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eBuilding on the geodynamic and geochemical framework outlined above, we now return to the idea that the very first lifeforms were simple encapsulated RNA-based entities. Unlike modern cellular life, which integrates DNA, RNA, and proteins in a highly interdependent system, a hypothesized RNA organism would have been a minimalist self-replicating unit, potentially consisting of one or a few RNA strands capable of template-directed replication and rudimentary catalysis, captured within a porous proto-cellular structure\u003csup\u003e\u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e43\u003c/span\u003e\u003c/sup\u003e. The core attributes of such an RNA organism stem from RNA's inherent versatility. Key to the RNA World argument is that experimental reconstructions show that RNA can form ribozymes - enzymatic RNAs - that catalyze their own replication, albeit with low fidelity and efficiency\u003csup\u003e\u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e44\u003c/span\u003e\u003c/sup\u003e. This autocatalytic capacity would have enabled the steps toward Darwinian evolution to take place in a prebiotic setting through heritable variation arising from replication errors, initially without the need for a separate translation apparatus\u003csup\u003e\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e\u003c/sup\u003e. Chirality is another pivotal requirement for stable RNA folding and function\u003csup\u003e\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e\u003c/sup\u003e, and was established early perhaps via prebiotic mechanisms such as asymmetric photolysis or mineral templating\u003csup\u003e\u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e45\u003c/span\u003e\u003c/sup\u003e. We emphasize encapsulation as a crucial component of this first living system and likely occurred with lipid vesicles or coacervates formed from amphiphilic molecules delivered by impactors or atmospheric chemistry and/or hydrothermal activity. The importance of encapsulation rests on the necessary compartmentalization to maintain chemical gradients and protect against dilution or degradation\u003csup\u003e\u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e43\u003c/span\u003e,\u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e46\u003c/span\u003e\u003c/sup\u003e. The first entities structurally resembled primitive protocells, but with RNA directing simple polymerization reactions and without the complexity of LUCA's ribosomal machinery.\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e\n\u003ch3\u003eRNA viruses are not the same as the RNA World organisms\u003c/h3\u003e\n\u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eNext, we draw a key distinction between hypothetical ancient cellular RNA organisms and modern RNA viruses. To be clear, RNA viruses are obligate intracellular parasites that hijack host cellular machinery for replication and lack independent metabolism\u003csup\u003e\u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e47\u003c/span\u003e\u003c/sup\u003e. The dearth of independent metabolism leads in part to the general consensus that viruses are not life forms. Phylogenetic analyses also suggest that RNA viruses emerged later, possibly as escaped genetic elements from DNA-based cells, rather than as relics of the RNA World\u003csup\u003e\u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e48\u003c/span\u003e,\u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e49\u003c/span\u003e\u003c/sup\u003e. This evolutionary divergence highlights the point that viruses do not serve as direct analogs for early RNA life, as they exhibit derived features like capsid proteins and host-specific adaptations not present in pre-LUCA scenarios.\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003ePseudo-heterotrophy in the RNA World\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eInstead of being virus-like, primordial RNA organisms were autonomous, proto-cellular systems capable of some kind of metabolism to sustain themselves in Hadean environments through direct interaction with geochemical resources and without relying on pre-existing cells. This is an important distinction; if the first RNA organisms were not autotrophic, neither could they have been heterotrophic \u003cem\u003esensu stricto\u003c/em\u003e. We refer here to the idea of such a simple and early passive \u0026ldquo;metabolism\u0026rdquo; for the first RNA life as \u003cem\u003epseudo-heterotrophic\u003c/em\u003e. This term recognizes the reliance of the first organisms for growth and reproduction on the availability of background abiotic production of organic molecules and building blocks generating in the Hadean environment. In these environments RNA World organisms may have been either free-living or attached to mineral or (rock) glass surfaces, or both.\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003eProposed sequence of events\u003c/h3\u003e\n\u003cp\u003eFigure \u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003e schematically reviews the key deviations between the different evolutionary stages of the emergent biosphere:\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003e \u003cb\u003eRNA World\u003c/b\u003e (Hypothesized origin): RNA was the primary information molecule, acting as both genotype (information storage) and phenotype (catalytic ribozymes). It is characterized by low stability and error-prone replication.\u003c/p\u003e \u003cp\u003e \u003cb\u003eRNP World\u003c/b\u003e (Ribonucleoprotein transition): RNA acted as a scaffold, recruiting amino acids/proteins to enhance stability and catalytic efficiency, forming complex ribonucleoprotein structures. This allowed for the early translation of genetic code.\u003c/p\u003e \u003cp\u003e \u003cb\u003eDNA World\u003c/b\u003e (Contemporary life): DNA replaced RNA as the primary, more stable, double-stranded genetic material, allowing for larger genomes, while proteins took over catalysis. DNA is distinct due to deoxyribose sugar and the base thymine.\u003c/p\u003e\n\u003ch3\u003eA contemporary RNA/RNP hidden biosphere?\u003c/h3\u003e\n\u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eCould extant RNA or RNP organisms still be lurking around in the present biosphere? Despite extensive metagenomic surveys of diverse environments - from deep-sea vents to human microbiomes - no evidence exists for separate and independent RNA-based cellular life somewhere in the background of the biosphere\u003csup\u003e\u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e50\u003c/span\u003e\u003c/sup\u003e. That said, few if any targeted searches have been conducted to search for such organisms. We recommend that such searches be undertaken. Recent discoveries, such as obelisks - short, circular RNA elements associated with bacterial hosts in the human gut - represent virus-like entities but depend on microbial cells for propagation and do not constitute autonomous organisms. Similarly, viroids, which are naked RNA pathogens of plants, lack coding capacity and require host polymerases\u003csup\u003e\u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e51\u003c/span\u003e\u003c/sup\u003e. The persistence of some kinds of RNA World remnants is instead evident in conserved cellular components, such as ribozymes in the spliceosome and RNase P, and the RNA-centric core of the ribosome all which hint at an ancient RNA-dominated phase\u003csup\u003e\u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e52\u003c/span\u003e,\u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e53\u003c/span\u003e\u003c/sup\u003e. The absence of extant RNA cells aligns with selective pressures favoring the RNA-to-DNA transition, as RNA's chemical instability \u0026ndash; most importantly due to its 2'-hydroxyl (2\u0026rsquo;-OH) group rendering it prone to hydrolysis \u0026ndash; would have limited long-term viability in evolving biospheres\u003csup\u003e\u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e54\u003c/span\u003e,\u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e56\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eThis conceptualization of a (proto)cellular RNA organism as a transient, rudimentary precursor sets the foundation for exploring Hadean environmental constraints and metabolic innovations that likely shaped its existence and eventual replacement.\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e \u003cdiv id=\"Sec11\" class=\"Section2\"\u003e \u003ch2\u003eChemical vulnerabilities of the RNA/RNP World\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eThe hypothetical RNA organisms described in the preceding section, characterized by reliance on RNA for both information storage and catalysis, were sensitive to the physicochemical conditions of the Hadean Earth. While the geodynamic models and geochemical evidence outlined earlier indicate that biocompatible conditions - with liquid water, organic precursors, and energy gradients - were established before 4.3 Gyr ago, the inherent instability of RNA imposes stringent environmental constraints on where and how such life could have persisted\u003csup\u003e\u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e54\u003c/span\u003e,\u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e56\u003c/span\u003e\u003c/sup\u003e. These limits arise from RNA's chemical vulnerabilities, including susceptibility to hydrolysis, photodegradation, and metal-ion-mediated cleavage, which would have confined viable niches to protected microenvironments capable of mitigating these stressors.\u003c/p\u003e \u003cp\u003eCentral to these constraints is RNA's lability in aqueous environments, often termed the \"water paradox\" in prebiotic chemistry: water is essential for biomolecular interactions yet promotes backbone hydrolysis via the 2\u0026rsquo;-OH group, with half-lives ranging from hours to days under neutral pH and ambient temperatures. Elevated temperatures exacerbate this, as RNA unfolding and degradation accelerate above ~\u0026thinsp;60\u0026ndash;80\u0026deg;C, rendering high temperature hydrothermal settings improbable for sustained RNA replication despite their potential for organic synthesis\u003csup\u003e\u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e56\u003c/span\u003e\u003c/sup\u003e. Furthermore, Hadean atmospheric greenhouse forcing after large impacts plausibly warmed the surface\u003csup\u003e\u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e30\u003c/span\u003e\u003c/sup\u003e. It is also hypothesized that variable production of reduced gases such as H\u003csub\u003e2\u003c/sub\u003e and CH\u003csub\u003e4\u003c/sub\u003e along with residual heat pulses from late accretion impacts further prolonged warm to hot surface conditions throughout the Hadean\u003csup\u003e\u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e29\u003c/span\u003e,\u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e31\u003c/span\u003e\u003c/sup\u003e. If surface temperatures were high (50\u0026ndash;70\u0026deg;) at that formative time\u003csup\u003e\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e\u003c/sup\u003e, only cooler refugia - such as subsurface aquifers or polar regions - would have offered thermal stability to RNA organisms. Moreover, stochastic short-lived environmental fluctuations, including periodic local high-temperature spikes from local impacts or regional volcanism, could disrupt RNA oligomer concentrations by 20\u0026ndash;40%, as modeled in resource-constrained simulations of prebiotic systems\u003csup\u003e\u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e57\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eUltraviolet (UV) radiation from the young Sun, intensified by both the activity of our star in its youth and the lack of an effective ozone layer in the early atmosphere, presents another formidable barrier, causing photodamage to nucleobases and strand breaks\u003csup\u003e\u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e58\u003c/span\u003e\u003c/sup\u003e. Solar UV fluxes were estimated to be 10\u0026ndash;100 times higher in the Hadean than today, sufficient to degrade exposed RNA within minutes to hours, necessitating shielding mechanisms like simple pigment-like structures, mineral adsorption, submersion in turbid waters\u003csup\u003e\u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e59\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eBoth pH extremes further limit RNA viability: acidic conditions (pH\u0026thinsp;\u0026lt;\u0026thinsp;5) accelerate hydrolysis, while highly alkaline settings (pH\u0026thinsp;\u0026gt;\u0026thinsp;10) may favor nucleotide synthesis but risk deamination; thus, mildly alkaline hydrothermal systems (pH 8\u0026ndash;10) emerge as plausible crucibles for the RNA World, as they could facilitate RNA polymerization on minerals or rock glasses to stabilize oligomers against dilution and degradation\u003csup\u003e\u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e60\u003c/span\u003e,\u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e61\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eMetal ions, abundant in Hadean oceans from crustal leaching and impact delivery, further add to this complexity: divalent cations like Mg\u003csup\u003e2+\u003c/sup\u003e are required for ribozyme folding and catalysis but can also promote phosphodiester cleavage at concentrations above ~\u0026thinsp;10 mM\u003csup\u003e62\u003c/sup\u003e. This dual role of Mg\u003csup\u003e2+\u003c/sup\u003e suggests that low-metal environments, perhaps in freshwater ponds hosted by emergent land as previously inferred from zircon oxygen isotopic data\u003csup\u003e\u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e37\u003c/span\u003e\u003c/sup\u003e, would have been more conducive to starting off an RNA World. Such environments allow for wet-dry cycles that concentrate reactants without excessive ion interference. Salinity poses additional challenges, as high ionic strength disrupts RNA secondary structures, favoring dilute or brackish settings over hypersaline basins. Debates persist regarding optimal locales, with submarine hydrothermal vents offering geochemical energy and mineral catalysis but risking thermal and pH instabilities\u003csup\u003e\u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e63\u003c/span\u003e\u003c/sup\u003e, as well as dilution of prebiotically useful components. This contrasts with warm springs or evaporative ponds on land surfaces that enable cyclic dehydration for polymerization\u003csup\u003e\u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e46\u003c/span\u003e\u003c/sup\u003e and favor concentration. Recent models highlight fluctuating conditions that mirror Hadean impact-driven perturbations: these impose temporal limits, with RNA persistence reliant on episodic stabilization rather than continuous equilibrium\u003csup\u003e\u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e57\u003c/span\u003e\u003c/sup\u003e. Such environmental boundaries shaped not only the distribution of RNA life but also the selective pressures that determined its functional capabilities, as discussed in the following section on metabolic styles.\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec12\" class=\"Section2\"\u003e \u003ch2\u003eHadean metabolic styles\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eThe environmental constraints delineated for RNA organisms, coupled with their rudimentary nature as self-replicating ribozyme systems, imply that their metabolic capabilities were inherently limited and intimately tied to the geochemical disequilibria of the Hadean Earth. In the RNA World framework, metabolism would have been orchestrated by ribozymes catalyzing essential reactions for self-maintenance and replication, drawing on prebiotic organic pools or in situ synthesis to sustain nucleotide monomers and energy equivalents\u003csup\u003e\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e,\u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e64\u003c/span\u003e\u003c/sup\u003e. These proto-metabolic styles likely spanned a continuum from pseudo-heterotrophic exploitation of exogenous organics - delivered via impacts or atmospheric photochemistry - to nascent autotrophic pathways leveraging hydrothermal redox gradients, with cooperative networks emerging to overcome individual catalytic inefficiencies\u003csup\u003e\u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e39\u003c/span\u003e,\u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e65\u003c/span\u003e\u003c/sup\u003e. Besides the proposed concept of protocells absorbing prebiotically produced monomers, another scenario could include the absorption of prebiotic compounds such as formamide, cyanamide, or glycolaldehyde by the protocells from the environment, with ribozymes facilitating their condensation into nucleotides or energy-rich intermediates\u003csup\u003e\u003cspan citationid=\"CR66\" class=\"CitationRef\"\u003e66\u003c/span\u003e\u003c/sup\u003e. For instance, non-enzymatic reactions amplified by RNA catalysis mimic aspects of the formose reaction, generating sugars like ribose under fluctuating wet-dry conditions in ponds on land, thereby fueling oligomer assembly without complex enzymatic cascades. These processes would predate the appearance of carbon fixation from CO\u003csub\u003e2\u003c/sub\u003e. This opportunistic style aligns with the dilute, variable Hadean surface environments, where RNA's catalytic promiscuity - enabling a single ribozyme to perform multiple reactions - compensated for low substrate specificity and turnover rates\u003csup\u003e\u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e56\u003c/span\u003e\u003c/sup\u003e. Such dependence, however, on external organics by pseudo-heterotrophy would have been vulnerable to depletion. This tension ultimately favors selection for more self-sufficient systems.\u003c/p\u003e \u003cp\u003eAutotrophic inclinations, particularly in alkaline hydrothermal vents, represent a complementary style wherein RNA organisms may have harnessed geochemical energy for carbon fixation and reduction\u003csup\u003e\u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e63\u003c/span\u003e\u003c/sup\u003e. Primitive versions of the Wood\u0026ndash;Ljungdahl pathway, driven by H\u003csub\u003e2\u003c/sub\u003e and CO\u003csub\u003e2\u003c/sub\u003e across mineral membranes, could have been ribozyme-assisted to produce acetyl thioesters as primitive energy currencies akin to acetyl-CoA\u003csup\u003e\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u003c/sup\u003e. In this scenario, metal cofactors (e.g., Fe-S clusters, or transition metals, like nickel and cobalt) are integrated with ribozymes to catalyze reductive carboxylation, bridging geochemistry to biochemistry in what has been termed a \"semi-enzymatic\" network\u003csup\u003e\u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e65\u003c/span\u003e\u003c/sup\u003e. Similarly, segments of the reverse tricarboxylic acid cycle might have operated abiotically with RNA enhancing efficiency, generating organic acids like pyruvate for nucleotide precursors under mild alkaline, reducing conditions. Such deep ancient pathways, rooted in Hadean vent chemistry modulated by what we can tell about the nature of the earliest crust, reinforces that concept of a metabolism-replication coupling where RNA replicators collectively sustained monomer pools, as modeled in surface-bound or vesicular communities\u003csup\u003e\u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e67\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eCooperative dynamics further characterized RNA metabolic styles, with replicator ensembles forming hypercycles or compartmentalized groups to ensure complete catalytic coverage\u003csup\u003e\u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e67\u003c/span\u003e,\u003cspan citationid=\"CR68\" class=\"CitationRef\"\u003e68\u003c/span\u003e\u003c/sup\u003e. On mineral surfaces, spatial structuring mitigated replicators, allowing metabolic completeness through group selection, while proto-cellular encapsulation intensified this by linking replication to shared metabolism. Such networks, potentially incorporating peptides (short proteins) for enhanced catalysis and stabilization, laid the groundwork for evolutionary refinement without preempting the genetic takeover by DNA.\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec13\" class=\"Section2\"\u003e \u003ch2\u003eThe road to LUCA ran through an RNP World\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eUnlike the classical RNA World hypothesis, which posits a stage dominated solely by catalytic RNA molecules, the RNP World emphasizes the subsequent or concomitant coevolution and integration of RNA with peptides and proteins into functional ribonucleoprotein assemblies\u003csup\u003e\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e,\u003cspan citationid=\"CR69\" class=\"CitationRef\"\u003e69\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e70\u003c/span\u003e\u003c/sup\u003e. The RNP World was therefore an intermediate stage where RNA catalysis and primitive peptide synthesis formed a system with greater catalytic versatility, structural stability, and evolutionary potential than either RNA or peptide alone. The central tenet is that RNPs emerged when RNA molecules and short peptides began to create organized, reproducible interactions that conferred catalytic robustness and information transfer advantages relative to RNA. This coevolutionary framework appears to overcome critical limitations of the RNA World model, particularly the chemical instability of RNA under prebiotic conditions particular to the Hadean Earth, and the limited catalytic repertoire of ribozymes compared to protein enzymes.\u003c/p\u003e \u003cp\u003eAt the molecular level, the RNP World is characterized by several key features which differentiate it from the hard RNA World. First, the Peptidyl Transferase Center (PTC) of the ribosome and proto-tRNA concatenation systems are proposed as early organizing structures that could bootstrap coded peptide formation and establish a primitive translation apparatus\u003csup\u003e\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e,\u003cspan citationid=\"CR69\" class=\"CitationRef\"\u003e69\u003c/span\u003e\u003c/sup\u003e. These proto-ribosomal assemblies may have provided a platform for the evolution of the genetic code and the gradual refinement of translation fidelity. Second, ribosomal RNAs and proteins appear to have undergone incremental accretion and coevolution, with small subunit processivity features predating the PTC catalytic core, implying a gradualist build-up of modern ribosomes from simpler RNP ancestors\u003csup\u003e\u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e70\u003c/span\u003e\u003c/sup\u003e. Interestingly, this structural phylogenetic evidence suggests that the ribosome itself is a molecular fossil preserving the evolutionary history of the RNP World.\u003c/p\u003e \u003cp\u003eLike RNA organisms, RNP organisms likely also possessed short, structured RNA genomes that functioned both as genetic material and catalysts, with heritable replication mediated by ribozymes or peptide-assisted RNA polymerases\u003csup\u003e\u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e70\u003c/span\u003e,\u003cspan citationid=\"CR71\" class=\"CitationRef\"\u003e71\u003c/span\u003e\u003c/sup\u003e. The inherent chemical instability of ribonucleotides under physiological conditions would have favored short RNA molecules with extensive secondary and tertiary structure, which could be stabilized through association with cationic or hydrophobic peptides\u003csup\u003e\u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e72\u003c/span\u003e,\u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e73\u003c/span\u003e\u003c/sup\u003e. Proto-tRNAs and tRNA concatenates are hypothesized to have served dual roles as adaptors for primitive peptide synthesis and as modular building blocks for early genes\u003csup\u003e\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e,\u003cspan citationid=\"CR69\" class=\"CitationRef\"\u003e69\u003c/span\u003e\u003c/sup\u003e. This tRNA-centric model of genetic organization suggests that the operational RNA code - the assignment of amino acids to specific RNA structures - preceded and scaffolded the emergence of the triplet genetic code.\u003c/p\u003e \u003cp\u003eThe catalytic machinery of RNP organisms were built around ribozyme cores performing essential functions such as RNA replication, peptide bond formation, and RNA processing\u003csup\u003e\u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e72\u003c/span\u003e\u003c/sup\u003e. Ancient ribozymes like RNase P RNA and PTC-like motifs provided key catalytic activities\u003csup\u003e\u003cspan citationid=\"CR74\" class=\"CitationRef\"\u003e74\u003c/span\u003e\u003c/sup\u003e, while associated proteins or short peptides progressively improved catalytic efficiency and substrate recognition\u003csup\u003e\u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e72\u003c/span\u003e\u003c/sup\u003e. Experimental evidence demonstrates that short cationic and hydrophobic peptides can adsorb onto RNA, stabilize secondary structures, and enhance the catalytic rates of polymerase ribozymes and other catalytic RNAs\u003csup\u003e\u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e70\u003c/span\u003e,\u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e73\u003c/span\u003e\u003c/sup\u003e. We posit that these wild environmental peptide-RNA interactions became more efficient over time through a positive feedback loop: RNA-encoded peptides enhance RNA catalysis, which in turn enables more efficient peptide synthesis and the evolution of longer, more complex proteins.\u003c/p\u003e \u003cp\u003eNon-canonical nucleoside chemistry provides additional support for RNA-peptide coevolution. Experiments have shown that peptide synthesis can occur directly on RNA scaffolds through non-canonical nucleoside linkages, producing peptide-RNA chimeras that demonstrate plausible prebiotic routes to integrated RNA-peptide systems and proto-translation chemistry\u003csup\u003e\u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e70\u003c/span\u003e\u003c/sup\u003e. Such chimeric molecules may have been the first entities capable of both information storage and catalytic function, bridging the gap between simple self-replicating molecules and modern cells, between RNA/RNP and the DNA/LUCA.\u003c/p\u003e \u003cp\u003eThe functional units of RNP organisms were likely ribonucleopeptide complexes and proto-ribosomal assemblies that combined RNA scaffolds with small proteins or peptides into integrated catalytic factories\u003csup\u003e\u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e70\u003c/span\u003e\u003c/sup\u003e. These RNP complexes would have operated within membrane-bound cells either free living or attached to mineral surface microenvironments, which concentrated reactants and protected fragile RNA molecules from degradation. The population structure of early RNP organisms may have been communal rather than clonal, with ensembles of diverse RNA sequences and peptide libraries creating an innovation-rich milieu characterized by frequent horizontal gene transfer and recombination. This genetic promiscuity accelerated evolutionary innovation by allowing beneficial mutations and molecular inventions to spread rapidly through the population.\u003c/p\u003e \u003cp\u003eThe transition from RNP-based organisms to modern DNA-protein cells involved multiple interconnected processes: the emergence of sophisticated protein catalysts, the invention of DNA as a stable genetic storage medium, and the refinement of the translation system to its modern form. The evolution of complex proteins from simple peptides proceeded through a feedback cycle in which improving translation allowed RNA-encoded peptides to fold into more effective RNA-binding and enzymatic proteins, which in turn enabled more efficient replication and expansion of genetic information. This positive feedback would have driven the gradual replacement of ribozyme catalysts by protein enzymes, as proteins offered superior catalytic versatility, specificity, and evolvability. Ancestral protein folds could have arisen from short peptides initially selected for RNA-binding and structural support, which subsequently acquired enzymatic functions through gene duplication and divergence\u003csup\u003e\u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e73\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eThe ribosome itself underwent a complex evolutionary trajectory from primitive PTC/tRNA systems to the multi-subunit molecular machine found in modern cells\u003csup\u003e\u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e70\u003c/span\u003e\u003c/sup\u003e. Structural and phylogenetic analyses reveal that small subunit components linked to mRNA binding and translational processivity likely evolved before the large subunit catalytic center, facilitating improvements in translation fidelity and the expansion of the genetic code\u003csup\u003e\u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e70\u003c/span\u003e\u003c/sup\u003e. The accretion model of ribosomal evolution, supported by comparative structural phylogenetics, suggests that ribosomal RNA and protein components were added incrementally, with each addition conferring selective advantages in translation speed, accuracy, or regulatory capacity.\u003c/p\u003e \u003cp\u003eTheoretical analyses that integrate biochemical plausibility, structural data, and evolutionary logic increasingly favor an early RNA-protein (RNP) stage as more feasible than a pure RNA World leading directly to a DNA World. Models of genetic code origin that link proto-tRNAs, PTC formation, and the operational/anticodon code provide mechanistic pathways for the emergence of coded translation within an RNP framework\u003csup\u003e\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e,\u003cspan citationid=\"CR69\" class=\"CitationRef\"\u003e69\u003c/span\u003e\u003c/sup\u003e. These models demonstrate that the key innovations of molecular biology - replication, transcription, and translation- emerged through the coevolution of RNA and peptide components, rather than requiring a purely RNA-based precursor stage.\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec14\" class=\"Section2\"\u003e \u003ch2\u003eDawn of the DNA World\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eThe metabolic adaptations of RNA organisms to RNP organisms, as constrained by Hadean geochemistry and reliant on ribozyme networks, likely persisted for a relatively geologically brief (ca. 150 Myr) interval before yielding to DNA-based heredity. This is most strongly evidenced by the phylogenetic placement of LUCA. Integrating molecular clock analyses with geochronological data, these studies constrain the RNA and RNP Worlds\u0026rsquo; duration to approximately 100\u0026ndash;200\u0026nbsp;million years\u003csup\u003e\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e,\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e\u003c/sup\u003e. This compressed timeline reconciles rapid prebiotic assembly in post-impact reducing atmospheres\u003csup\u003e\u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e29\u003c/span\u003e\u003c/sup\u003e facilitating nucleotide synthesis via HCN and nitriles with the swift evolutionary ascent to LUCA's complexity which encompasses a\u0026thinsp;~\u0026thinsp;2.5 Mb genome encoding\u0026thinsp;~\u0026thinsp;2,600 proteins\u003csup\u003e\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e,\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u003c/sup\u003e. The RNA World (primordial) relied on self-replicating RNA for both information and catalysis, the RNP World featured RNA acting with proteins for enhanced function, and the DNA World utilizes stable, double-stranded DNA for storage with protein enzymes for metabolism (Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eAs previously mentioned, divergence time estimates, calibrated against microbial fossils and gene duplications predating LUCA, consistently position this ancestor in the late Hadean, with a median age of 4.2 Gyr and ranges extending from 3.94 to 4.52 Gyr. This is an important datum in our argument because the RNA-to-DNA handover would have occurred amid ongoing late accretion, where impact-driven perturbations accelerated selection for more stable genetic systems without necessitating protracted stasis. Evidence from ancestral gene reconstructions further supports this rapidity: the innovation of ribonucleotide reductases and thymidylate synthases - enabling deoxyribonucleotide production from RNA precursors - likely arose within this 100\u0026ndash;200 Myr window, potentially via ribozyme-to-protein catalysis shifts\u003csup\u003e\u003cspan citationid=\"CR75\" class=\"CitationRef\"\u003e75\u003c/span\u003e\u003c/sup\u003e. Stepwise models propose a three-phase progression from autocatalytic RNA networks to template-directed replication, aligning with the swift integration of DNA for enhanced fidelity\u003csup\u003e\u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e65\u003c/span\u003e,\u003cspan citationid=\"CR76\" class=\"CitationRef\"\u003e76\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eBiogeodynamic contextualization reinforces this brevity: with emergent land and hydrological cycles fostering diverse niches, RNA populations could diversify rapidly, but Hadean environmental stresses \u0026ndash; UV fluxes, thermal excursions and ion imbalances \u0026ndash; would impose stringent limits on scalability, favoring the genetic transition. This temporal framework, while not precluding lingering RNA entities in refugia, demarcates the RNA World's eclipse as a pivotal threshold, driven by environmental pressures that ultimately favored DNA-centric life.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec15\" class=\"Section2\"\u003e \u003ch2\u003eWhy DNA prevailed over RNA and RNP\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eThe circumscribed duration of the RNA World, as inferred from phylogenetic and geodynamic evidence, stresses the evolutionary imperatives that propelled the ascendancy of DNA as the principal genetic material. We have reviewed how RNA's versatility enabled the inception of replication and metabolism, but its intrinsic limitations - chemical instability, propensity for misfolding, and error-prone replication - rendered it ill-suited for sustaining increasingly complex biospheres, paving the way for DNA's selective dominance\u003csup\u003e\u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e54\u003c/span\u003e,\u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e55\u003c/span\u003e\u003c/sup\u003e. We propose that this was not abrupt but emerged through incremental biochemical innovations exploiting DNA's more fit and robust attributes that were driven by the Hadean environmental pressures favoring enhanced genomic reliability and scalability.\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec16\" class=\"Section2\"\u003e \u003ch2\u003eRNA has inferior chemical and structural stability\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eThe lack of 2'-hydroxyl group is a disadvantage to RNA. Whereas DNA contains deoxyribose, the 2'-OH group is still present in RNA's ribose sugar. This -OH group makes RNA highly susceptible to hydrolysis and rapid degradation. DNA\u0026rsquo;s backbone is far less prone to cleavage, making it a more robust repository for genetic data.\u003c/p\u003e \u003cp\u003eAs a double helix, the structure of DNA protects the nitrogenous bases inside the structure. This configuration shields information from chemical damage (e.g., UV light, hydrolysis).\u003c/p\u003e \u003cp\u003eUracil is used in RNA and because DNA instead uses thymine (5-methyluracil), it provides additional stability and is more resistant to photochemical mutations compared to uracil.\u003c/p\u003e \u003cp\u003eTemperatures above about 50 ˚C, and pH\u0026thinsp;\u0026gt;\u0026thinsp;8 are detrimental to RNA structures. These are also unstable at seawater salinities.\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec17\" class=\"Section2\"\u003e \u003ch2\u003eRNA has lower replication fidelity and repairability\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eDNA replication is far less error-prone than RNA replication, allowing for the stable transmission of much larger genomes. This is because the complementary double-stranded structure allows for error-checking and repair. If one strand is damaged, the other can serve as a template for repair.\u003c/p\u003e \u003cp\u003eCytosine often breaks down into uracil (deamination). In DNA, the presence of uracil can be easily identified as foreign and repaired. In an RNA world, uracil is a natural base, making such repairs impossible\u003csup\u003e\u003cspan citationid=\"CR78\" class=\"CitationRef\"\u003e78\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec18\" class=\"Section2\"\u003e \u003ch2\u003eRNA is unable to support larger genomes\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eSince DNA is less likely to self-fold into complex 3D structures (a common issue for RNA), it is more suitable as a template. This allows DNA to form long, linear, or circular structures (chromosomes) that can store vast amounts of information without getting tangled or degraded.\u003c/p\u003e \u003cp\u003eDue to its stability, DNA can act as a long-term, passive hard drive for genetic information, while RNA is better suited for short-term, active roles in protein synthesis.\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec19\" class=\"Section2\"\u003e \u003ch2\u003eThe RNP World is a short-lived compromise\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eSeveral key advantages exist for the transitional RNP World over the classic RNA World to DNA World scenario, primarily by addressing the inherent instability of pure RNA and its limited catalytic repertoire. The RNP World posits that early biological systems formed a partnership between RNA and peptides, allowing them to overcome the limitations of relying on RNA alone. Such a partnership increased stability by protecting RNA from degradation. As RNA is notoriously chemically unstable and prone to hydrolysis the binding of proteins (or peptides) to RNA in RNP complexes shielded RNA from degradation. Peptides can provide structural stability to RNA molecules, allowing them to form complex, durable shapes that would be impossible for single-stranded RNA on its own\u003csup\u003e\u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e70\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eWhile RNA can act as a catalyst (ribozyme), its repertoire is limited compared to protein enzymes. Peptides introduce a wider range of chemical properties (hydrophobic and hydrophilic) that enhance the catalytic rate of reactions. Compared to RNA alone, RNP complexes combine the best of both worlds: the information storage of RNA and the efficient catalysis of proteins. The RNP transition also solves the dilemma of which came first -functional proteins or informational RNA - by proposing they co-evolved as partners from the earliest stages. Amino acids (the building blocks of proteins) were available in early Earth conditions and could have served as cofactors, enabling faster synthesis of RNA-related molecules compared to an RNA-only environment.\u003c/p\u003e \u003cp\u003eThe RNP World is supported by modern biology, as the ribosome (which synthesizes all proteins) is itself a complex ribonucleoprotein, with RNA acting as the catalyst. It provides a more realistic, gradual pathway from simple prebiotic chemistry to the complex, DNA-based life we know today, rather than requiring a sudden, improbable jump to a fully functional RNA-only system.\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec20\" class=\"Section2\"\u003e \u003ch2\u003eBottlenecks\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eForemost among DNA's advantages is its heightened chemical stability, stemming from the absence of the 2'-hydroxyl group on deoxyribose\u003csup\u003e\u003cspan citationid=\"CR78\" class=\"CitationRef\"\u003e78\u003c/span\u003e\u003c/sup\u003e. In contrast to RNA's labile single-stranded forms, DNA's canonical double-helix structure further bolsters durability, enabling the archiving of longer sequences with reduced degradation rates \u0026ndash; essential for accommodating the ~\u0026thinsp;2.5 Mb genome inferred for LUCA\u003csup\u003e\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e\u003c/sup\u003e. Computational analyses reveal that DNA strands exhibit folding free energies approximately tenfold higher than RNA counterparts, minimizing secondary structures that impede template accessibility and replication fidelity. This stability facilitated the separation of informational roles, with DNA serving as a robust repository while RNA retained catalytic and intermediary functions, alleviating the dual burden on RNA in primordial systems.\u003c/p\u003e \u003cp\u003eMechanistic pathways for this shift likely involved the prebiotic or early biotic synthesis of deoxyribonucleotides from ribonucleotide precursors, catalyzed by proto-enzymes or ribozymes akin to modern ribonucleotide reductases\u003csup\u003e\u003cspan citationid=\"CR75\" class=\"CitationRef\"\u003e75\u003c/span\u003e\u003c/sup\u003e. Non-enzymatic templating of DNA strands on RNA scaffolds, followed by enzymatic replication via emergent RNA-dependent DNA polymerases or reverse transcriptase-like activities, would have initiated chimeric RNA-DNA systems. The incorporation of thymine over uracil further enhanced error detection. \u003cem\u003eIn silico\u003c/em\u003e simulations and experimental models demonstrate that such genetic takeovers could occur under fluctuating conditions, with DNA-enriched protocells outcompeting RNA-only variants through superior heritability and reduced mutational load\u003csup\u003e\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e\u003c/sup\u003e. These general advantages created the first bottleneck effect \u0026ndash; where RNA organisms drastically fell behind DNA organisms in the competition, creating a decline in their numbers, allowing DNA based life to flourish.\u003c/p\u003e \u003cp\u003eSelective forces in Hadean milieux \u0026ndash; ion imbalances, thermal cycles, and impact-induced disruptions \u0026ndash; amplified these benefits, as populations with DNA-mediated heredity exhibited greater resilience and adaptive potential, culminating in the DNA-protein World's establishment by LUCA. This creates the second bottleneck, driven by the environmental factors. This evolutionary pivot not only resolved the RNA World's vulnerabilities but also enabled the diversification that defines contemporary life. The transition from RNA to DNA genomes remains one of the most enigmatic events in early evolution. Several scenarios have been proposed to explain this shift. One prominent hypothesis invokes viral or retroelement-mediated introduction of reverse transcription and ribonucleotide reductase activities, which would have enabled the synthesis of DNA nucleotides and the copying of RNA genomes into more stable DNA forms. Alternative models suggest independent inventions of DNA synthesis in separate lineages, driven by selection for more stable genetic storage in increasingly complex organisms\u003csup\u003e\u003cspan citationid=\"CR78\" class=\"CitationRef\"\u003e78\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eImportantly, the transitions to DNA-based genomes and fully proteinaceous enzyme systems need not have occurred synchronously across all lineages. Evidence supports parallel or independent transitions in different lineages descended from communal RNP progenitors, with some lineages adopting DNA earlier than others\u003csup\u003e\u003cspan citationid=\"CR78\" class=\"CitationRef\"\u003e78\u003c/span\u003e\u003c/sup\u003e. This mosaic pattern of evolutionary innovation is consistent with the progenote concept, which views early life as a diverse community of organisms with partially formed, error-prone genetic and translational systems that gradually refined through natural selection and horizontal gene transfer.\u003c/p\u003e \u003cp\u003eThe relationship between the RNP World and the Last Universal Common Ancestor (LUCA) is central to understanding the deep evolutionary history of life. Rather than viewing LUCA as a single cell with modern biochemistry, recent analyses frame LUCA as a descendant of RNP-era populations, possibly representing a complex, genetically redundant community shaped by its RNP legacy. Several lines of evidence suggest that LUCA may have been a complex, possibly mesophilic community with extensive genetic redundancy and traces of RNA-based heredity consistent with RNP ancestry\u003csup\u003e\u003cspan citationid=\"CR78\" class=\"CitationRef\"\u003e78\u003c/span\u003e\u003c/sup\u003e. This community model resolves several paradoxes in LUCA reconstruction, including the presence of apparently incompatible biochemical features and the difficulty of reconciling LUCA\u0026rsquo;s inferred complexity with the simplicity expected of early life. We argue that LUCA was a community rather than a single organism, which means horizontal gene transfer among community members would have homogenized many genes while allowing lineage-specific innovations to persist in different subpopulations.\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e \u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eThe RNA World hypothesis, which elevates RNA to being the primordial genetic and catalytic material, provides a framework for life's inception amid the Hadean Earth's geodynamic environment. Life's emergence coincided with the rapid assembly of RNA replicators in clement niches on Hadean Earth. These niches were circumscribed by late accretion bombardment and modulated by early hydrological cycles that supplied organics and energy gradients\u003csup\u003e\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e,\u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e37\u003c/span\u003e\u003c/sup\u003e. The RNA organisms were minimalist, autonomous protocells distinct from modern viruses that navigated stringent environmental limits. These included the water paradox, UV fluxes, and ionic perturbations, confining them to protected hydrothermal or terrestrial settings where ribozyme catalysis enabled heterotrophic scavenging or nascent autotrophy\u003csup\u003e\u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e55\u003c/span\u003e,\u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e63\u003c/span\u003e,\u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e65\u003c/span\u003e\u003c/sup\u003e. Metabolic styles, from opportunistic formose-like reactions to proto-Wood\u0026ndash;Ljungdahl pathways in cooperative networks, underscored RNA's versatility but also its fragility, with low fidelity and instability constraining scalability\u003csup\u003e\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e,\u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e67\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eThe RNP World hypothesis provides a coherent and mechanistically plausible waystation from the RNA World to DNA genomes and the emergence of LUCA. By emphasizing the coevolution of RNA and peptides into integrated functional systems, the RNP World model addresses key limitations of the pure RNA World hypothesis and offers testable predictions about the molecular organization, catalytic capabilities, and evolutionary trajectories of early organisms. The ribosome, as a molecular fossil preserving the architecture of ancient RNP assemblies, stands as a testament to this deep evolutionary history.\u003c/p\u003e \u003cp\u003eThis brevity of the RNA and RNP Worlds - spanning 100\u0026ndash;200 Myr before LUCA's advent at ~\u0026thinsp;4.2 Gyr ago \u0026ndash; is dictated by the intense environmental pressures of the Hadean Earth\u0026rsquo;s surface, where late accretion impacts and geochemical fluctuations selected for DNA's superior stability, fidelity, and informational capacity. The transition to DNA, mediated by ribonucleotide reduction and chimeric templating, resolved RNA's vulnerabilities, enabling the DNA-protein paradigm that underpinned LUCA's genomic sophistication and the biosphere's persistence\u003csup\u003e\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eOur analysis does not in any way diminish the RNA World's foundational role but frames its demise as an evolutionary imperative: Without the handover to DNA, life's trajectory toward complexity might have stalled, as recent ribozyme reconstructions affirm RNA's catalytic prowess yet highlight its inadequacy for long-term evolvability in dynamic environments.\u003c/p\u003e \u003cp\u003eOriginal insights from this synthesis suggest that the RNA and RNP Worlds\u0026rsquo; fall was not merely a biochemical improvement but a biogeodynamic upgrade that potentially happens on exoplanets with similar accretionary histories. For instance, if Hadean-like impacts accelerated nucleotide synthesis and selection, then biocompatible worlds with clement surfaces around young Sun-like (F,G,K) stars might also be expected to host at least fleeting RNA phases. Conversely, this transience challenges the orthodox \"Hard RNA World\u0026rdquo; variant, by implying a continuum where peptides and DNA co-emerged earlier than presumed, as evidenced by studies on RNA-sulfur interactions fostering proto-peptides\u003csup\u003e\u003cspan citationid=\"CR66\" class=\"CitationRef\"\u003e66\u003c/span\u003e\u003c/sup\u003e. Future research should refine models integrating these findings, perhaps through \u003cem\u003ein vitro\u003c/em\u003e experiments with protocells enclosing RNA strands that are exposed to RNA monomers in solution to test the \u003cem\u003epseudo-heterotrophy\u003c/em\u003e concept. Ultimately, the RNA World's swift eclipse illuminates the resilience of early life rather than its fragility, transforming a hypothesized precursor into life\u0026rsquo;s first actor in Earth's biogeodynamic narrative.\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e"},{"header":"Materials and Methods","content":"\u003cp\u003e \u003cdiv class=\"BlockQuote\"\u003e \u003cp\u003eFigure \u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e, shows the instantaneous percent of lithosphere molten over time, was generated using a three-dimensional impact bombardment model of the Hadean Earth\u0026rsquo;s lithosphere\u003csup\u003e\u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e31\u003c/span\u003e,\u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e33\u003c/span\u003e,\u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e34\u003c/span\u003e\u003c/sup\u003e. A stochastic cratering model populated the surface with craters according to the Brasser late accretion chronology\u003csup\u003e\u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e28\u003c/span\u003e\u003c/sup\u003e, delivering a total mass of 0.57 wt% Earth (\u0026asymp;\u0026thinsp;3.4 \u0026times; 10\u003csup\u003e22\u003c/sup\u003e kg) between 4.5 and 3.5 Ga, with a size-frequency distribution of rocky impactors\u003csup\u003e\u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e31\u003c/span\u003e\u003c/sup\u003e analogous to the main asteroid belt and impact velocity distribution derived from dynamical simulations\u003csup\u003e\u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e31\u003c/span\u003e\u003c/sup\u003e. Simulations were initiated from either a pre-existing crust (baseline) or a global magma ocean formed by the Moon-forming impact\u003csup\u003e\u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e27\u003c/span\u003e\u003c/sup\u003e. Basaltic target properties were adopted (surface temperature 20\u0026deg;C, geothermal gradient 70\u0026deg;C km\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e, density 3000 kg m\u003csup\u003e\u0026minus;\u0026thinsp;3\u003c/sup\u003e, heat capacity 800 J kg\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e \u0026deg;C\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e, thermal conductivity 2.5 W m\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e \u0026deg;C\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e, solidus 1100\u0026deg;C). Melting was defined as crustal material being heated above the basalt liquidus temperature of ~\u0026thinsp;1250\u0026deg;C, while accounting for the latent heat of fusion of basalt at ~\u0026thinsp;400 kJ kg\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e in the energy balance. At each time step the model computed the volume of lithosphere exceeding the criteria for melting and expressed this as a percentage of the total lithosphere volume, yielding the instantaneous molten fraction for the two initial states. The data to reproduce Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e is provided in Supplementary data file Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e_data.xls.\u003c/p\u003e \u003c/div\u003e \u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAcknowledgments\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding:\u003c/strong\u003e This work was supported by the ERC Horizon Europe funding programme in support of the Synergy Grant - GEOASTRONOMY, grant agreement number 101166936 (to S.J.M.. O.A.), funding from the Research Center for Astronomy and Earth Sciences (CSFK), an MTA Center of Excellence, in Budapest, Hungary (to A.M., O.A. and S.J.M.) and the Institute of Paleobiology Polish Academy of Sciences (to B.K.). The idea for this paper was an outcome of the Biogeodynamics COST Action CA23150 “EUROBiG”, supported by the European Cooperation in Science and Technology.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthor contributions:\u003c/strong\u003e Conceptualization: A.M., S.J.M., B.K., and O.A. Methodology: A.M., S.J.M.. Software: O.A. Data curation: O.A.. Formal analysis: A.M., S.J.M. Investigation: A.M., B.K.. Validation: A.M., B.K., S.J.M.. Visualization: S.J.M.. and O.A.. Writing—original draft: A.M., S.J.M., O.A. and B.K.. Writing—review and editing: A.M., O.A., B.K. and S.J.M.. Resources: S.J.M.. Funding acquisition: S.J.M.. Project administration: S.J.M.. Supervision: S.J.M. and B.K.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompeting interests:\u003c/strong\u003e The authors declare that they have no competing interests.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eData and materials availability:\u003c/strong\u003e All data are available in the main text or the supplementary materials.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eMaher, K. A. \u0026amp; Stevenson, D. J. Impact frustration of the origin of life. \u003cem\u003eNature \u003c/em\u003e\u003cstrong\u003e331\u003c/strong\u003e, 612\u0026ndash;614 (1988). https://doi.org/10.1038/331612a0\u003c/li\u003e\n\u003cli\u003eMoody, E. R. R. \u003cem\u003eet al.\u003c/em\u003e The nature of the last universal common ancestor and its impact on the early Earth system. \u003cem\u003eNat. Ecol. 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Direct \u003c/em\u003e\u003cstrong\u003e10\u003c/strong\u003e, 67 (2015). https://doi.org/10.1186/S13062-015-0096-Z\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"scientific-reports","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"scirep","sideBox":"Learn more about [Scientific Reports](http://www.nature.com/srep/)","snPcode":"","submissionUrl":"","title":"Scientific Reports","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"stoa","reportingPortfolio":"Scientific Reports","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"RNA World, RNP World, Origin of Life, Last Universal Common Ancestor, Hadean","lastPublishedDoi":"10.21203/rs.3.rs-9212823/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-9212823/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eThe RNA World is an early developmental stage in biology before the DNA World. If the first life on Earth began as a cellular RNA life-form which later transitioned to a ribonucleoprotein (RNP) organism, it did not stay that way for long. The last universal common ancestor (LUCA) of all contemporary DNA life seems to have existed already by the late Hadean eon (ca. 4.2 Gyr ago). Understanding what could have driven the evolution of the RNA/RNP World to the DNA World at this early time necessitates a biogeodynamic contextualization of the co-evolution of life and the Hadean Earth environment. Here we draw a connection between recent findings about LUCA and its habitat to make inferences about the earliest biological entities. We argue that environmental conditions on Hadean Earth motivated the transition to a DNA world. Selection pressures on minimalist autonomous RNA/RNP protocells with ribozyme-driven heterotrophic or nascent autotrophic metabolisms favored stability and fidelity. Our findings do not preclude RNA or RNP organisms at the time of the LUCA.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eShort description\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eA swift demise of the RNA World underscores the hardiness of early life on Hadean Earth rather than its vulnerability to extinction.\u003c/p\u003e","manuscriptTitle":"Whence the demise and fall of the RNA World?","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2026-04-25 03:26:56","doi":"10.21203/rs.3.rs-9212823/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Revision requested","date":"2026-05-14T13:31:44+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-05-13T21:10:21+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-04-29T01:02:31+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"312864298689977410660735827179808536780","date":"2026-04-17T15:51:33+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"213842915635027122771285493087490075380","date":"2026-04-17T14:32:16+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2026-04-16T19:38:38+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2026-04-15T16:56:08+00:00","index":"","fulltext":""},{"type":"editorInvited","content":"","date":"2026-04-15T16:45:55+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2026-04-10T19:27:34+00:00","index":"","fulltext":""},{"type":"submitted","content":"Scientific Reports","date":"2026-04-10T18:35:02+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"scientific-reports","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"scirep","sideBox":"Learn more about [Scientific Reports](http://www.nature.com/srep/)","snPcode":"","submissionUrl":"","title":"Scientific Reports","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"stoa","reportingPortfolio":"Scientific Reports","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"a30e60b3-c215-4f4e-9e8a-3ef5497eb49a","owner":[],"postedDate":"April 25th, 2026","published":true,"recentEditorialEvents":[{"type":"decision","content":"Revision requested","date":"2026-05-14T13:31:44+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2026-05-13T21:10:21+00:00","index":20,"fulltext":""}],"rejectedJournal":[],"revision":"","amendment":"","status":"in-revision","subjectAreas":[{"id":66536428,"name":"Biological sciences/Ecology"},{"id":66536429,"name":"Earth and environmental sciences/Ecology"},{"id":66536430,"name":"Biological sciences/Evolution"},{"id":66536431,"name":"Biological sciences/Genetics"},{"id":66536432,"name":"Biological sciences/Molecular biology"}],"tags":[],"updatedAt":"2026-05-14T13:39:58+00:00","versionOfRecord":[],"versionCreatedAt":"2026-04-25 03:26:56","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-9212823","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-9212823","identity":"rs-9212823","version":["v1"]},"buildId":"XKTyCvWXoU3ODBz1xrDgd","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}