Co-evolving N-Fe redox processes controlled iron minerals in banded iron formation

Co-evolving N-Fe redox processes controlled iron minerals in banded iron formation | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Article Co-evolving N-Fe redox processes controlled iron minerals in banded iron formation Hongchen Jiang, Liuqin Huang, Yanlong Dong, Linxin Li, Nicole Nie, and 4 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-3724120/v1 This work is licensed under a CC BY 4.0 License Status: Under Review Version 1 posted You are reading this latest preprint version Abstract Biogeochemical cycles in the Precambrian ocean responded to the co-evolution of biosphere (microorganisms) and the physicochemical structure (e.g., redox, temperature) of the ocean, which closely link to the enigma of banded iron formations (BIFs) that primarily triggered by massive Fe(II) oxidation under anoxic-hypoxic condition for two-billon years (~3.8-1.8 Ga). The current Fe(II) oxidation models, however, rarely consider the effects of the evolution of coupled biogeochemical cycles on secular succession (shifting from magnetite to hematite) of dominant iron minerals in BIFs. Here, we investigated the evolution of coupled Fe-N redox processes under the simulated Precambrian ocean conditions, and propose a dynamic model for the origin of iron mineral succession in BIFs: During the early-mid Archean, NO 2 - was mainly produced by nitrification in the oceans of warm-hot temperatures (>50-60 o C), which favored the primary precipitation of Fe(II)-Fe(III) oxides (magnetite) and silicates (cronstedtite) in the early BIFs. Subsequently, the cooling and oxygenation of paleo-ocean near the GOE promoted the input of both NO 2 - and NO 3 - , resulting in co-precipitation of an increasing amount of Fe(III) minerals (goethite and lepidocrocite as precursors of hematite). This dynamic N-Fe coupling model explains the observed secular transition of iron mineral phases in BIF deposition. Earth and environmental sciences/Biogeochemistry/Element cycles Earth and environmental sciences/Planetary science/Mineralogy Figures Figure 1 Figure 2 Figure 3 Introduction The early Precambrian ocean, especially during Archean to Paleoproterozoic, was characterized by low oxygen, rich reductants, and probably warm-hot temperature (>50 ℃, probably higher than 70 ℃) conditions 1 , but irreversibly evolved into oxic and temperate conditions in the late Neoproterozoic 2 . Although many details remain controversial about the evolutionary history of the ocean 3 , there is no doubt that large environmental changes, especially the gradual cooling and stepwise oxygenation of the ocean, fundamentally shaped the physiochemical structure (e.g., ferruginous to stratified euxinic to oxic) of the oceans and the microbial world (e.g., thermophilic anaerobes evolving into mesophilic aerobes). The evolving marine microbiota thereby would have been responsible for the changing biogeochemical reactions (especially for redox sensitive elements such as N, Fe, C) and their products over geological time 4, 5 . A major event closely intertwined with paleo-ocean biogeochemical evolution is the massive deposition of BIFs from the seawater column through extensive Fe(II) aq oxidation during the early Precambrian (dominantly during 3.8-1.8 Ga) 6 . The geochemical, isotopic and mineralogical records of BIFs exhibit temporal and spatial variations. For example, the average valence state of Fe in BIFs gradually increased over time, because of a shift in dominant Fe minerals from magnetite (especially >2.9 Ga) to hematite (particularly after the Neoarchean) 7 , suggesting that Fe(II) oxidation process evolved. Currently photo- and/or O 2 -dependent Fe(II) oxidation in the shallow euphotic zone of paleo-oceans is widely considered to account for BIF precipitation, but this model is difficult to explain the intriguing mineralogical or geochemical changes of BIFs over time 8 . How the evolving biogeochemical processes affect Fe(II) oxidation pathways and the resulting mineral products across anoxic-oxic transition was rarely considered in the previous models. The early anoxic ocean (> 3.0 Ga) was filled with ammonium-replete ferruginous waters, where the main anaerobic biological processes included N 2 reduction to NH 4 + and Fe(II)-based anoxic photosynthesis (photoferrotrophy) 9, 10 . At this time, vertical profiles of NH 4 + and Fe(II) in paleo-oceans were uniform (Fig. 1a). As oxygenic photosynthesis emerged to gradually consume reductants 11 , the uniformly reducing water column evolved into a heterogeneous one due to the developments of redoxcline and chemocline (Fig. 1b) 12, 13 . These developments would have greatly changed the pathways of Fe(II) oxidation 14 . Under the rising redox state of the paleo-oceans, NH 4 + would be continuously oxidized to nitrogen oxyanions (NO x - , mainly NO 2 - and NO 3 - ) even in anoxic waters 15, 16 that can be dated back at least to the Mesoarchean 12, 17 . As a result, an intermediate nitrogenous zone gradually developed between the upper oxidizing surface water and the lower ferruginous water (Fig. 1b) 18, 19 . This nitrogenous zone is commonly found in oxygen minimum zone (OMZ) of modern oceans and ferruginous lakes, both regarded as the analogues of the hypoxic Precambrian ocean 20, 21 . This nitrogenous layer is crucial to Fe(II) oxidation because it would act as a redoxcline/chemocline barrier by consuming O 2 and CO 2 from above via nitrification and by oxidizing the upwelling Fe(II) aq from below via N-dependent Fe(II) oxidation (general reaction: Fe(II) + NO x - → Fe(III) + N 2 ) 22, 23 . The N-dependent Fe(II) oxidation mechanism would greatly decrease the dominance of the traditional photo- and/or O 2 -dependent Fe(II) oxidation by spatially separating the reactants required in previously proposed Fe(II) oxidation mechanisms (Fig. 1b) 8 . Interestingly, the peak deposition of BIFs at 2.7-2.4 Ga, after the onset of aerobic nitrification (and the presence of nitrogenous layer) 24 but before the remarkable rise of atmospheric O 2 marked as the Great Oxygenation Event (GOE, 2.4-2.2 Ga) 25, 26 , argues for the potential importance of coupled N-Fe redox cycling to BIF deposition. However, direct evidence is lacking. Here we hypothesize that an active, biologically-driven N-Fe redox process develops around the nitrogenous layer in the shallow water (Fig. 1) that is responsible for Fe(II) oxidation and substantially contributes to BIF formation. To test this hypothesis, we investigated how the evolution of coupled processes of Fe(II) oxidation and N redox cycling affect the formation of BIF-related mineral products under the simulated Precambrian ocean conditions. Response of nitrification and denitrification to temperature cooling Ammonia, formed abiotically on early Earth (e.g., volcanic, lightning, bolide 30 , 31 , serpentinization of ultrabasic rocks 32 ) and biotically at later times 10 , was the predominant form of fixed N pool in the early reducing ocean (Fig. 1 a) 9 , 33 . Aerobic ammonia oxidation, which can occur under extremely low oxygen level (at nM level) 34 or even in anoxic waters 16 , was dated back to at least ~ 3.0 Ga 13 and would have triggered the N redox processes by supplying NO x - species to the ancient oceans (Fig. 1 b), but it was scarcely considered by current biogeochemical models. For example, at a low O 2 level, the end products of the N redox processes were highly sensitive to temperature, probably via the effect of temperature on microbial functions and incomplete nitrification and denitrification processes in response to temperature changes. To simulate the N redox processes in a gradually cooling hypoxic Precambrian ocean, nitrifying and denitrifying microbial consortia were enriched from hot springs in Xizang and Yunnan Provinces, China, which span broad geochemical and temperature gradients (Fig. S1 , Table S1 and S2). The reason to use hot spring as an analog of Precambrian ocean was because key physicochemical properties in hot springs, such as low contents of oxygen and organic carbon, and high contents of Fe, N and Si, are similar to those of the paleo-oceans 35 . Furthermore, the microorganism-dominated community in hot springs, including many thermophilic ancestors, is a good analog of the simple biosphere on the early earth 36 . Nitrifying enrichments were first recovered from diverse hot springs ranging from 75 o C to 30 o C (Fig. S2 and S3). Interestingly, the dominant product of NH 4 + oxidation gradually shifted from NO 2 - to NO 3 - in response to a temperature decrease, with a temperature cross-over at 60 − 50 o C (Fig. 2 a) regardless of the spring water geochemistry. Consistently, ammonia oxidizing archaea (AOA, performing NH 4 + oxidation to NO 2 - ) were ubiquitous in the enrichments, with thermophilic Nitrosocaldales being dominant in higher temperature (> 40 o C) and Nitrososphaerales at lower temperature. Nitrite-oxidizing bacteria (NOB), mainly Nitrospirales , that can oxidize NH 4 + /NO 2 - to NO 3 - were only revealed at lower temperature (< 40 o C, Fig. S3). This observation is consistent with previous studies in that AOA were detected at temperature up to 90 o C, but most NOB isolates, if not all, were active under 60 o C 37 , 38 , 39 , 40 . Therefore, a transition of fixed N from NH 4 + to NO 2 - and then to NO 3 - may have occurred as a result of cooling of the Precambrian ocean. NO x - generated by nitrification may be reduced by canonical denitrification under reducing condition. Therefore, canonical denitrifying consortia under the same temperature gradient were enriched to explore the stability of produced NO x - under different temperature conditions (Fig. S4 and S5). Interestingly, accumulation of NO 2 - resulting from NO 3 - reduction significantly decreased with temperature cooling (Fig. 2 b), i.e., higher temperature favored production of NO 2 - . This was well illustrated in one representative hot spring flow channel, in which denitrifying consortia stoichiometrically accumulated NO 2 - from NO 3 - reduction at 65 o C, less at 55 o C, and undetectable at 50 o C (Fig. S5). The denitrifying consortia were dominated by Hydrogenobacter (more abundant at high temperature) and Thermus (Fig. S4), two types of common denitrifying bacteria in hydrothermal habitats 41 , 42 . In fact, incomplete denitrification of NO 3 - and accumulation of NO 2 - were commonly observed in thermophilic cultivations 43 , 44 , 45 and oxygen-depleted waters 46 . Therefore, NO 2 - accumulation from ammonia nitrification or nitrate reduction would be a substantial source of N species especially under elevated temperatures. In summary, an evolving N inventory would have developed in the hypoxic cooling Precambrian ocean. A NO 2 - -dominant nitrogenous layer may gradually form in the shallow water by incomplete nitrification (NH 4 + →NO 2 - ) and denitrification (weak NO 2 - reduction), especially in the early high temperature (> 50–60 o C) ocean. With the cooling of the ancient ocean, NO 3 - was gradually produced in larger quantities through complete nitrification at lower temperature (especially < 50 o C), leading to the pervasive mixture of NO 2 - and NO 3 - in the ocean, although an increasing proportion of NO x - was also reduced into gaseous N species (e.g., N 2 O, N 2 ) through denitrification. Temperature-driven Fe(II) oxidation coupled with NO reduction In addition to production of NO x - via nitrification and partial removal via denitrification, they can be reduced by an alternative and even more abundant electron donor in the ferruginous Precambrian ocean–the rich Fe(II) 20 , 27 . Fe(II) can be chemically oxidized by NO 2 - reduction (known as chemodenitrification) and/or microbially induced by NO 3 - reduction (known as nitrate-dependent Fe(II) oxidation, NDFO). Vertically, the NO x - -rich layer just overlayed the lower Fe(II)-rich ferruginous water, providing an opportunity for chemo- and microbial denitrification. However, how NO x - -dependent Fe(II) oxidation occurred under the scenario of the evolving NO x - pool and cooling temperature are unclear. Therefore, chemical and biological induced NO x - - dependent Fe(II) oxidation was simulated under a broad range of temperature schemes (25-75 o C), with consideration of co-effects on mineral formation of HCO 3 - and dissolved Si that were rich in the Precambrian ocean 47 , 48 , 49 . Chemodenitrification was tested at temperatures ranging from 25 o C to 75 o C, which showed higher Fe(II) oxidation and NO 2 - reduction (both the rate and extent) by higher temperature (Fig. S6). Mineral formation also changed systematically with temperature cooling (summarized in Table 1 ). In the absence of dissolved Si, magnetite that can reach micrometer-scale size was the main or even only mineral product at temperature higher than 55 o C (Fig. S7, S9-a3, a4, b3, b4; Fig. S8-a, b). When HCO 3 - was present, magnetite started to form at 40 o C (Fig. S7, S9-b2; Fig. S8-a). In contrast, lepidocrocite and goethite predominantly precipitated at temperatures of 25 and 40 o C when supplemented with Cl - and HCO 3 - , respectively (Fig S7, S9-a1, a2, b1, b2). Addition of dissolved Si did not prevent Fe(II) oxidation by NO 2 - but significantly altered the iron mineral phases and crystallization, as the main minerals turned to be weakly crystallized cronstedtite (empirical formula: Fe 2 + 2 Fe 3 + 2 SiO 5 (OH) 4 , an Fe(III)-containing greenalite-like serpentine) and greenalite while a small part of magnetite only existed at higher temperature (Fig. S7, S8, S9-c). Biologically induced NO x - - dependent Fe(II) oxidation was first tested with the use of a typical thermophilic NO 3 - -reducing isolate from a Xizang hot spring, Thermus sp., at 55 o C and 75 o C. Fe(II) was effectively oxidized by NO 3 - reduction at both temperatures, regardless of the presence of Si (Fig. S10). NO 2 - was accumulated from NO 3 - reduction without Fe(II) (Fig. S10a), but it was not observed in the presence of Fe(II) (Fig. S10-c, d), suggesting that Fe(II) oxidation either consumed the produced NO 2 - or bypassed it during the NO 3 - reduction pathway. Magnetite was the only mineral product at both temperatures without Si (Fig. S11-a1, a2). When Si was present, cronstedtite was the dominant well-crystalline mineral at 55 o C (Fig. S11-b1), accompanied with some greenalite (Fig. S8-d). Magnetite was co-precipitated with cronstedtite and greenalite at 75 o C (Fig. S11-b2, Fig. S8-e). Notably, microbially formed silicate minerals in Si-amended treatment were more crystalline compared to those formed by chemodenitrification (compared Figs. S11-b and S7-c). Many of these minerals tightly encrusted the cell surface (Fig. S12), suggesting that microbial activity greatly stimulated mineral crystallization. Three representative denitrification consortia, enriched from a spring channel (Fig. S1 -b1) of different temperatures but similar water chemistry, were tested for their performance in Fe(II) oxidation. The three consortia were dominated by Hydrogenobacter sp. at high temperature (65 o C) and by Thermus sp. at lower temperature (55 and 50 o C, Fig, S4). Fe(II) oxidation occurred in consortia at higher temperature (> 50 o C) when NO 2 - was produced as a byproduct of NO 3 - reduction (Fig. S1 3-b, c), but did not occur without consortia or in consortia of lower-temperature (50 o C) (Fig. S1 3-a), suggesting that Fe(II) was oxidized metabolically and/or chemically by NO 2 - . The mixture of cronstedtite and magnetite was the main mineral products (Fig. S1 1-c), similar to that formed by pure Thermus sp. strain in the presence of Si, probably due to the fact that the hot spring water contained a considerable amount of Si (Table S1 ). Mineral particles, especially for the cronstedtite formed by the denitrifying consortia (Fig. S1 4), however, were larger in size than those formed by pure Thermus strain, perhaps due to slower Fe(II) oxidation rate or interspecies interaction in the microbiota. In summary, higher temperature (over ~ 50 o C) favored the precipitation of Fe(II)-Fe(III)-mixed minerals, especially magnetite, either via chemical or biological Fe(II) oxidation when coupled with NO x - reduction; in comparison, lower temperature was more beneficial to the formation of Fe(III) minerals (Table 1 ). This variation in mineralogy in response to a temperature gradient is consistent with the trend observed in natural BIFs, that is, early BIFs (at higher temperature) were dominated by magnetite, and later (at lower temperature) gradually shifted to hematite (as partially summarized in Table S3). In addition, the presence of denitrifying microbial consortia tends to promote the formation of magnetite at lower temperature, with a higher proportion and better crystallinity relative to their absence, suggesting the importance of direct (mediate N-Fe reactions) and indirect (such as providing mineral adsorption sites for crystallization) biological effects on iron mineral precipitation in BIFs. Table 1 Iron minerals precipitated by chemical and biological N-Fe redox coupling under temperature gradient a Temperature ( o C) Reactions Iron minerals Lepidocrocite Goethite Magnetite Silicates (Cronstedtite, Greenalite) 55 Chemodenitrification - + + + + + + + Microbial NDFO - - + + + + + + + a Summarized based on the mineral composition in Figs. S7-S9, S11, S12, S14. More signs of “+” denote higher abundance. Black “+” symbols show the mineral composition in Si-absent treatments, while red “+” symbols show that in Si-rich systems; “-” denotes not detectable, and “/” denotes not tested in this study. Coupled N-Fe redox cycles for the mineralogical succession of BIFs Reconstruction of the effect of biogeochemical evolution on BIF across geological timescale is extremely difficult due to the uncertainty of changes in key environmental factors. For example, oxygen level is a crucial factor determining whether Fe(II) oxidation is influenced by oxic or anoxic processes. However, it is difficult to determine the evolution of oxygen level in paleo-oceans with heterogeneous chemical structures, despite the widespread consensus of an overall rise of oxygen in the atmosphere of the early Earth. In comparison, temperature cooling is more predictable. From a long-term geological perspective, temperature cooling of the paleo-oceans is an indisputable fact, although the absolute magnitude of cooling is still controversial. Nevertheless, the cooling trend of temperature of the Archean-Proterozoic oceans would greatly reshape the structure and functional composition of microbial communities, thereby altering biogeochemical processes in the ocean, including the N and Fe cycling and BIF deposition. In the present work, by integrating all the results, we developed a four-stage evolution scenario for the coupled N-Fe redox processes, providing a possible explanation for the secular changes of iron mineral precipitation in BIFs in the Archean-Paleoproterozoic ocean (Fig. 4): Small scale BIFs (i.e., with typical laminated Si-rich and Fe-rich layers) began to deposit as early as 3.8 Ga. ago. 50 The ocean was hot (most probably higher than 55 o C, even over 75 o C) 1 , 47 , 51 , highly reducing, and almost devoid of any microbial activity (if any). Iron minerals in these oldest BIFs are overwhelmingly dominated by magnetite, accompanied by some Fe-silicates, such as grunerite, but few contain hematite 52 . During this prebiotic era, abiotic N 2 fixation was the main process of introducing a low flux of fixed N, (initially NO 2 - ) (~ 10 6 -10 10 mol N∙year -1 or even higher), into the ferruginous ocean 30 , 53 . The NO 2 - would be rapidly reduced through chemical oxidation of Fe(II) especially at high temperature, followed by precipitation of iron in the form of magnetite (2NO 2 - + 9Fe 2+ + 16HCO 3 - →N 2 + 3Fe 3 O 4 + 8H 2 O + 16CO 2 , as shown in Fig. S6-c), and/or cronstedtite in the presence of Si. Therefore, although NO 2 - would not be accumulated to a considerable concentration, its abiotic supply was sufficient to precipitate a large proportion of the oldest BIFs (totally ~ 10 11 -10 12 mol Fe in the Paleoarchean BIFs estimated by the BIF deposit size and average 20 wt% Fe content, Fig. 3 a). Moreover, the primary production of Fe(II)-Fe(III)-mixed minerals (magnetite, silicates) eases the vexatious requirement of a reduction step of ferric iron precursors (e.g., ferrihydrites), as proposed previously 54 . This scenario offers a reasonable explanation for the higher abundance of magnetite in the early BIFs 7 . After the Mesoarchean, deposition of BIFs increased slightly, until the Neoarchean. Magnetite is still the predominant iron mineral in most BIFs (particularly > 2.9 Ga) 7 . During the Mesoarchean, biological N 2 fixation bloomed and greatly enlarged the NH 4 + flux to the ocean 9 , 10 . Microbial oxidation of NH 4 + may also emerge as early as in the Mesoarchean 55 , as AOA could have oxidized ammonia at extremely low levels of O 2 or even in the anoxic water 15 , 16 . Moreover, local “oxygen oasis”, due to the emerging oxygenic photosynthesis 55 , may have gradually stimulated NH 4 + oxidation 12 . Therefore, microbial nitrification provided additional NO x - flow, mainly NO 2 - , as the temperature was still likely much higher than modern oceans (over 50 o C, as indicated in Figs. 2 a and 4). With the increase of NO 2 - flux, chemical oxidation of Fe(II) by NO 2 - , which primarily forms magnetite and cronstedtite, was still the predominant process of coupled N-Fe processes. This scenario offers an explanation for the increase of magnetite-dominant BIFs volume (totally ~ 10 14 -10 15 mol Fe in Mesoarchean BIFs as estimated by the BIFs deposit size and average 20 wt% Fe content, Fig. 3 b) 6 . BIF deposition increased significantly after the Neoarchean, reaching a peak from the mid-Neoarchean to the early Paleoproterozoic (2.7–2.4 Ga), right before GOE. Intriguingly, hematite content increased dramatically in these BIFs, especially after 2.6 Ga, suggesting that certain important transition of biogeochemical processes might have occurred and significantly affected the Fe redox cycle. Indeed, the oxygenation of surface water was more pervasive at this time, which greatly stimulated aerobic nitrification and further increased the NO x - flux. For example, the extremely positive excursions in δ 15 N was observed in the 2.7–2.5 Ga sediments, which was interpreted as a great rise in N loss via coupled nitrification-denitrification processes 56 , 57 . Therefore, the abundant NO x - might be extensively reduced by Fe(II) oxidation considering the super-large BIF deposition during this period. However, as temperature continued to decrease (lower than 50 o C), microbial nitrification of NH 4 + would produce a mixture of NO 2 - and NO 3 - with an increasing share of NO 3 - . With the increased NO x - pool/flux, Fe(II) oxidation coupled with microbial NO 3 - reduction and chemical NO 2 - reduction produced a mineral assemblage of magnetite, silicates, and Fe(III) hydroxides (i.e., goethite, lepidocrocite, Fig. 3 c). Over time at certain temperature and pressure, these ferric hydroxides can transform to hematite 58 . Furthermore, the relative dominance of Fe(III) hydroxides produced by N-Fe redox coupling would gradually increase at lower temperatures (Table 1 ), which offers a plausible explanation for the transition of magnetite-dominant to hematite-dominant BIFs during this period. A dramatic decrease or even stop of BIF deposition was observed after 1.8 Ga when the temperature further cooled down, suggesting a quiescence of Fe(II) oxidation at this time (Fig. 3 d). Two possible reasons may account for this transition. First, canonical nitrification-denitrification cycles might outcompete the coupled N-Fe cycles, due to rapid and complete oxidation of NH 4 + (into NO 3 - ) and complete reduction of NO 3 - to N 2 O and N 2 gases (Fig. S1 d, S4c) at low temperatures. Second, the development of an euxinic zone (S 2 - rich layer, caused by increased sulfate input from oxidative weathering of continental sulfides) between the nitrogenous and ferruginous layers provided an important reductant (i.e., S 2 - ) to consume NO x - and/or precipitate Fe(II) 59 , both of which would weaken the coupling of the N-Fe cycles. This scenario offers a possible explanation for the extremely low BIFs during the Meso- and Neoproterozoic (without considering the Rapitan IFs deposited during the Neoproterozoic). In summary, our proposed evolution model of the coupled N-Fe cycling processes, as a response to temperature decrease, provides a reasonable explanation for the successive change of abundance and mineralogy of BIFs. An important reason for the overlooked role of the coupled N-Fe cycles in the BIF formation in most previous studies is the assumption of the low accumulation of oxidative NO x - species in the reducing Precambrian ocean. However, we argue that the increasing flux and changing speciation of NO x - are extremely important for triggering extensive Fe(II) oxidation and mineral formation. A recent study found that the networked N-Fe reactions would provide substantial N 2 O emission and N burial (by association with Fe minerals) in the Precambrian marine ecosystem 60 , supporting the pervasive N-Fe reactions. Here we further demonstrated that N and Fe cycles could also be directly coupled to affect Fe mineralogy. In addition, our observed iron mineral assemblages formed by the dynamically evolving N-Fe coupling also have some other under-appreciated geological and environmental consequences, such as the bioavailability of N (via change of N speciation) and P (via adsorption to iron minerals) overtime, thereby controlling primary productivity and emission of greenhouse gasses N 2 O and CO 2 60 . Finally, further work is required for additional assessment of the contribution of N-Fe coupling to BIF deposition, which include, but not limited to, the competition by different Fe(II) oxidation pathways, quantitative impacts of other evolutionary factors (e.g., pH, Ca/Mg), and the N and Fe isotopic footprints recorded in geological archives in response to temperature gradients. Methods Thermophilic nitrification and denitrification consortia enrichment and analyses Hot springs in the geothermal fields in Tengchong, Yunnan Province (Rehai, Ruidian and Houqiao), China, with diverse temperature and geochemical gradients, were sampled in September 2019, August 2020 and November 2021. Xizang (Dagejia, Quzhuomu and Qucai) hot springs were sampled in August 2020 (detailed in the Supplemental text, Fig. S1 , Tables S1 and S2). Thermophilic nitrifying and denitrifying consortia were preliminarily enriched in the field. At each selected hot spring, spring water mixed with sediment suspension was aseptically injected into pre-autoclaved Balch glass bottles with needles, which served as medium and microbial inoculant. The bottles were filled with air for nitrification enrichment but degassed by N 2 gas for denitrification enrichment. The main reason for using hot spring water as a medium was to minimize any bias caused by defined media. However, enrichment was also performed with defined media 61 in representative hot springs to test the stability of nitrification and denitrification. NH 4 + and NO 3 - (final concentrations 0.5-1 mM) were amended as substrates for nitrifying and denitrifying cultures, respectively, and the bottles were incubated in situ for 3–5 days in hot springs to stimulate microbial growth. The in-situ enrichments were subsequently transported to laboratory at ambient temperature in less than a week. In the lab the enrichments were incubated in incubators with temperatures similar to the corresponding springs. The concentrations of NH 4 + , NO 2 - and NO 3 - were periodically monitored by spectrophotometric methods. The positive cultures that showed NH 4 + oxidation or NO 3 - reduction were then transferred to new media. Transfer continued for 2–5 times to obtain stable nitrification and denitrification consortia. Microbial compositions in successful enrichments were analyzed for representative temperatures (75 o C, 65 o C, 55 o C and 40 o C) by using the 16S rRNA gene pyrosequencing approach. Microbial and chemical analyses are provided in the SI. Fe(II) oxidation coupled with NO reduction (chemodenitrification) Fe(II) oxidation by NO 2 - reduction (NO 2 - + Fe 2+ → N 2 + Fe 3+ ) is also known as chemodenitrification. To mimic iron mineral formation by chemodenitrification under conditions of cooling and water chemistry rich in HCO 3 - and dissolved Si of the Precambrian ocean, four experimental sets were established at the temperature range of 25–75 o C (as listed in Table S4) with and without Si (2 mM 48 ). The reaction was buffered in PIPEs buffer to maintain the pH at 7, and the levels of Fe(II) (1 mM) and NO 2 - (0.2 mM) were selected to simulate their low concentrations in the Precambrian ocean and ensure enough mineral formation for analysis. The medium was degassed with pure N 2 gas on a gassing station, autoclaved, and sampled in an anaerobic glove box. Fe(II) and NO 2 - levels were regularly monitored and the final mineral products were collected for X-ray diffraction, scanning electronic microscopy, and Mössbauer analyses as detailed in the SI. Fe(II) oxidation coupled with NO 3 - reduction by Thermus sp. Microbial Fe(II) oxidation coupled with NO 3 - reduction (NO 3 - + Fe 2+ \(\underrightarrow{\varvec{c}\varvec{e}\varvec{l}\varvec{l}}\) N 2 /N 2 O/NO 2 - + Fe 3+ ) is common among denitrifying bacteria 62 . A typical thermophilic denitrifier, Thermus sp. isolated from Tibet hot spring (DGJ, 70 o C) and having a broad range of growth temperature (50–80 o C, optimal 60 o C), was used to test its capability of Fe(II) oxidation. Thermus sp. was grown in T5 medium (Table S5), which was then washed three times by 10 mM PIPEs buffer to remove any organic substrates. The collected Thermus sp. cells were used for NDFO test in a final concentration of ~ 1×10 7 cells per mL. The PIPES-buffered non-growth medium, the same as that for chemodenitrification, was used, with NO 2 - replaced by NO 3 - . Four experimental sets were established at two temperatures (55 o C and 75 o C) to compare the effects of cells and silica on mineral formation (Table S5). Fe(II) oxidation coupled with NO reduction by denitrifying consortia Three canonical denitrifying enrichment consortia from the same hot spring stream with different temperatures (DG1-1, DG1-2 and DG1-3 at 65, 60 and 50 o C, respectively, Fig. S1 ) were selected to test their potential capability on Fe(II) oxidation and mineral formation. The water collected from the source spring was used as the medium for all three consortia. Three experimental sets were established for each consortium to compare their effects on Fe(II) oxidation (Table S6): a) abiotic control without inoculation, b) Fe(II) + inoculated consortia to test any electron acceptor possibly present in the hot spring water itself, and c) NO 3 - + Fe(II) + inoculated consortia. Declarations Competing interests The authors declare no competing interests. Author contributions LH and YD contributed equally to conceptualization, data analysis and draft writing. LH, YD, LL, JY and LM performed data collection. LH, HJ and HD acquired fundings. LH, YD, HD and HJ wrote the original draft, and all authors reviewed and edited the manuscript. Acknowledgments This work was supported by the National Natural Science Foundation of China (NSFC- 42192503, 42172340, 42192500, 91951205), and the “Deep-time Digital Earth” Science and Technology Leading Talents Team Funds for the Central Universities for the Frontiers Science Center for Deep-time Digital Earth, China University of Geosciences (Beijing) (Fundamental Research Funds for the Central Universities; grant number: 2652023001)”. References McGunnigle JP, Cano EJ, Sharp ZD, Muehlenbachs K, Cole D, Hardman MF, et al. Triple oxygen isotope evidence for a hot Archean ocean. Geology 2022, 50(9): 991–995. Robert F, Chaussidon M. A palaeotemperature curve for the Precambrian oceans based on silicon isotopes in cherts. Nature 2006, 443(7114): 969–972. Blake RE, Chang SJ, Lepland A. 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Supplementary Files Huangetal.2023TableS3.Ironmineralsinbandedironformationsatdifferentgeologicaltime.docx Huangetal.2023NGSIsubmitted.docx Supplementary text, Tables and figures Cite Share Download PDF Status: Under Review Version 1 posted 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. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. 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-3724120","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":257532170,"identity":"3901bbbd-6820-4b06-acf5-1c7ea11162bc","order_by":0,"name":"Hongchen Jiang","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAAyElEQVRIiWNgGAWjYBACxmYQ0WAD4fGQoCWNBC0QfQ2HSdDC3M787OHXHeflDc4vYHzwto1B3pyww9jMjWXP3DbccOMBs+HcNgbDnQ0EtTCYSUu23U4wuHGATZq3jSHB4ABBLezfgFrOgbSw/yZSC4+Z5Me2AwkG5xvYmInVUibN2JZsOPMGY7PknHMShhsIaTHsP75N8mebnTzf+cMHP7wps5EnaIthAzCgwdEhkdgAIgmoBwJ5kON+gFj8hEwfBaNgFIyCEQsAuzpAJiVt0y0AAAAASUVORK5CYII=","orcid":"https://orcid.org/0000-0003-1271-7028","institution":"China University off Geosciences, Wuhan","correspondingAuthor":true,"prefix":"","firstName":"Hongchen","middleName":"","lastName":"Jiang","suffix":""},{"id":257532171,"identity":"b3c89035-d21b-4f48-bd50-26d7c6e242ed","order_by":1,"name":"Liuqin Huang","email":"","orcid":"","institution":"China University of Geosciences, Wuhan","correspondingAuthor":false,"prefix":"","firstName":"Liuqin","middleName":"","lastName":"Huang","suffix":""},{"id":257532172,"identity":"f1795b4e-f230-422a-b0bc-009800c80f4b","order_by":2,"name":"Yanlong Dong","email":"","orcid":"","institution":"China University of Geosciences, Wuhan","correspondingAuthor":false,"prefix":"","firstName":"Yanlong","middleName":"","lastName":"Dong","suffix":""},{"id":257532173,"identity":"049ce052-6eba-40bd-8150-35698a5bb582","order_by":3,"name":"Linxin Li","email":"","orcid":"","institution":"China University of Geosciences, Wuhan","correspondingAuthor":false,"prefix":"","firstName":"Linxin","middleName":"","lastName":"Li","suffix":""},{"id":257532174,"identity":"a1d816d6-c703-4d28-b6f8-7041691f2f05","order_by":4,"name":"Nicole Nie","email":"","orcid":"","institution":"Massachusetts Institute of Technology","correspondingAuthor":false,"prefix":"","firstName":"Nicole","middleName":"","lastName":"Nie","suffix":""},{"id":257532175,"identity":"22feca14-d334-4de0-8bc4-331253509805","order_by":5,"name":"Geng Wu","email":"","orcid":"","institution":"China University of Geosciences","correspondingAuthor":false,"prefix":"","firstName":"Geng","middleName":"","lastName":"Wu","suffix":""},{"id":257532176,"identity":"3139306f-e342-4291-a0bc-4d2b72cb2648","order_by":6,"name":"Jian Yang","email":"","orcid":"","institution":"China University of Geosciences","correspondingAuthor":false,"prefix":"","firstName":"Jian","middleName":"","lastName":"Yang","suffix":""},{"id":257532177,"identity":"c6cac4df-0ea2-40b9-a702-012e8ef40c50","order_by":7,"name":"Li Ma","email":"","orcid":"","institution":"China University of Geosciences, Wuhan","correspondingAuthor":false,"prefix":"","firstName":"Li","middleName":"","lastName":"Ma","suffix":""},{"id":257532178,"identity":"b5719fc9-9b94-4fb7-b620-ca0840f1282c","order_by":8,"name":"Hailiang Dong","email":"","orcid":"https://orcid.org/0000-0002-7468-1350","institution":"China University of Geosciences - Beijing","correspondingAuthor":false,"prefix":"","firstName":"Hailiang","middleName":"","lastName":"Dong","suffix":""}],"badges":[],"createdAt":"2023-12-08 07:10:51","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-3724120/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-3724120/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":49325397,"identity":"6b00d6b8-04f4-4ee9-88e7-6d8154947ae4","added_by":"auto","created_at":"2024-01-08 17:23:37","extension":"jpg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":87380,"visible":true,"origin":"","legend":"\u003cp\u003eSchematic depiction of vertical chemocline/redoxcline in the seawater columns and their effects on the distribution of major redox-sensitive geochemical species and N-Fe redox processes. Panel \u003cstrong\u003ea\u003c/strong\u003e: The early-middle Archean ocean was characterized by a vertically homogeneous water column that was rich in Fe(II) and NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e; Panel \u003cstrong\u003eb\u003c/strong\u003e:\u0026nbsp; Redox stratification gradually developed as a result of the rise of oxygenic photosynthesis, which created a mildly oxic surface water, a middle nitrogenous zone, which promoted the occurrence of nitrification-denitrification and N-dependent Fe(II) oxidation (NDFO), and a bottom ferruginous water. Vertical distributions of the N and Fe geochemical species are compiled from OMZ of modern oceans and ferruginous lakes, as well as from reconstructed Precambrian ocean\u003ca href=\"#_ENREF_6\" title=\"Konhauser, 2017 #94\"\u003e\u003csup\u003e6\u003c/sup\u003e\u003c/a\u003e\u003csup\u003e, \u003c/sup\u003e\u003ca href=\"#_ENREF_15\" title=\"Berg, 2015 #388\"\u003e\u003csup\u003e15\u003c/sup\u003e\u003c/a\u003e\u003csup\u003e, \u003c/sup\u003e\u003ca href=\"#_ENREF_20\" title=\"Swanner, 2020 #285\"\u003e\u003csup\u003e20\u003c/sup\u003e\u003c/a\u003e\u003csup\u003e, \u003c/sup\u003e\u003ca href=\"#_ENREF_21\" title=\"Scholz, 2018 #319\"\u003e\u003csup\u003e21\u003c/sup\u003e\u003c/a\u003e\u003csup\u003e, \u003c/sup\u003e\u003ca href=\"#_ENREF_22\" title=\"Scholz, 2016 #330\"\u003e\u003csup\u003e22\u003c/sup\u003e\u003c/a\u003e\u003csup\u003e, \u003c/sup\u003e\u003ca href=\"#_ENREF_27\" title=\"Michiels, 2017 #325\"\u003e\u003csup\u003e27\u003c/sup\u003e\u003c/a\u003e\u003csup\u003e, \u003c/sup\u003e\u003ca href=\"#_ENREF_28\" title=\"Bertagnolli, 2018 #438\"\u003e\u003csup\u003e28\u003c/sup\u003e\u003c/a\u003e\u003csup\u003e, \u003c/sup\u003e\u003ca href=\"#_ENREF_29\" title=\"Busigny, 2024 #444\"\u003e\u003csup\u003e29\u003c/sup\u003e\u003c/a\u003e.\u003c/p\u003e","description":"","filename":"floatimage1.jpg","url":"https://assets-eu.researchsquare.com/files/rs-3724120/v1/468a0c8d1d678e5ccd9ffa8a.jpg"},{"id":49325396,"identity":"2e9da289-2417-46cd-ad04-7ceb30051a68","added_by":"auto","created_at":"2024-01-08 17:23:36","extension":"jpg","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":121412,"visible":true,"origin":"","legend":"\u003cp\u003eVariations of nitrifying and denitrifying products in experiments by consortia from hot springs under different temperatures. Panel \u003cstrong\u003ea\u003c/strong\u003e: Conversion of\u003cstrong\u003e \u003c/strong\u003eNH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e into NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e (grey dots) and NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e (orange dots) by nitrifying consortia; Panel\u003cstrong\u003e b:\u003c/strong\u003e Conversion of NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e to NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e by denitrifying consortia. The shadows indicate 95% confident level of fittings.\u003c/p\u003e","description":"","filename":"floatimage2.jpg","url":"https://assets-eu.researchsquare.com/files/rs-3724120/v1/7b6ac81c32f7d000218e1216.jpg"},{"id":49325398,"identity":"9a5ca023-ffcb-468b-87b7-4367628994c8","added_by":"auto","created_at":"2024-01-08 17:23:37","extension":"jpg","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":347304,"visible":true,"origin":"","legend":"\u003cp\u003eSketch of N-Fe redox coupling for mineral deposition during different stages in Precambrian era. Panel \u003cstrong\u003ea\u003c/strong\u003e: In early prebiotic and hot ocean, N\u003csub\u003e2\u003c/sub\u003e was most abiotically fixed, resulting in a small flux of NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e in the ocean, which chemically oxidized Fe(II) into magnetite and/or Fe(II)-Fe(III) silicates to form small volume of BIFs; Panel\u003cstrong\u003e b\u003c/strong\u003e: NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e flux was enlarged \u0026nbsp;by microbial azotification, and a small part was nitrified \u0026nbsp;into NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e at elevated temperature (\u0026gt;~55 \u003csup\u003eo\u003c/sup\u003eC), which promoted chemodenitrification and deposition of magnetite and cronstedtite for a slightly larger scale of BIFs deposition; Panel\u003cstrong\u003e c\u003c/strong\u003e: near GOE, more oxidative state and lower temperature favored nitrification, leading to a\u0026nbsp; larger flux of NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e- \u003c/sup\u003e- NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e mixture in the nitrogenous layer, and more Fe(II) was both chemically oxidized by NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction and microbially oxidized by NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction to form ferric hydroxides (goethite) and mixed minerals of magnetite/cronstedtite, peaking in BIFs deposition; Panel\u003cstrong\u003e d\u003c/strong\u003e: stable chemoclines developed in the shallow waters, with euxinic layer sandwiching between upper nitrogenous layer and lower ferruginous zone near shore, which prevented NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e-reducing Fe(II) oxidation thereby; N redox was also largely decoupled with Fe(II) oxidation because canonical nitrification-denitrification cycle might overwhelm N-Fe coupling; Some ferric hydrates dominant minerals were produced via other possible pathways (indicated by the grey arrow in\u003cstrong\u003e \u003c/strong\u003epanel\u003cstrong\u003e d\u003c/strong\u003e) such as oxidation by oxygen.\u003c/p\u003e","description":"","filename":"floatimage3.jpg","url":"https://assets-eu.researchsquare.com/files/rs-3724120/v1/ab05c48fad7507f605fd56f2.jpg"},{"id":56716973,"identity":"47c8e2b2-8b90-45d2-9f42-7af18cf7cf18","added_by":"auto","created_at":"2024-05-18 21:03:22","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1249034,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3724120/v1/00fd55ca-02c9-4fb3-897e-fa9ad63aafb3.pdf"},{"id":49326268,"identity":"62488b5f-71ad-44b6-90e9-2b5bb4eb50f3","added_by":"auto","created_at":"2024-01-08 17:31:37","extension":"docx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":27861,"visible":true,"origin":"","legend":"","description":"","filename":"Huangetal.2023TableS3.Ironmineralsinbandedironformationsatdifferentgeologicaltime.docx","url":"https://assets-eu.researchsquare.com/files/rs-3724120/v1/c58d5a38911a3282cd37e01d.docx"},{"id":49325400,"identity":"c40ed9b1-1ea0-46ec-a63e-edecb53c20be","added_by":"auto","created_at":"2024-01-08 17:23:37","extension":"docx","order_by":2,"title":"","display":"","copyAsset":false,"role":"supplement","size":14393218,"visible":true,"origin":"","legend":"\u003cp\u003eSupplementary text, Tables and figures\u003c/p\u003e","description":"","filename":"Huangetal.2023NGSIsubmitted.docx","url":"https://assets-eu.researchsquare.com/files/rs-3724120/v1/d242b36cee08be14b900149b.docx"}],"financialInterests":"There is \u003cb\u003eNO\u003c/b\u003e Competing Interest.","formattedTitle":"Co-evolving N-Fe redox processes controlled iron minerals in banded iron formation","fulltext":[{"header":"Introduction","content":"\u003cp\u003eThe early Precambrian ocean, especially during Archean to Paleoproterozoic, was characterized by low oxygen, rich reductants, and probably warm-hot temperature (\u0026gt;50 ℃, probably higher than 70 ℃) conditions\u003csup\u003e1\u003c/sup\u003e, but irreversibly evolved into oxic and temperate conditions in the late Neoproterozoic\u003csup\u003e2\u003c/sup\u003e. Although many details remain controversial about the evolutionary history of the ocean\u003csup\u003e3\u003c/sup\u003e, there is no doubt that large environmental changes, especially the gradual cooling and stepwise oxygenation of the ocean, fundamentally shaped the physiochemical structure (e.g., ferruginous to stratified euxinic to oxic) of the oceans and the microbial world (e.g., thermophilic anaerobes evolving into mesophilic aerobes).\u0026nbsp;The evolving\u0026nbsp;marine microbiota thereby would have been responsible for the changing biogeochemical reactions (especially for redox sensitive elements such as N, Fe, C) and their products over geological time\u003csup\u003e4, 5\u003c/sup\u003e. A major event closely intertwined with paleo-ocean biogeochemical evolution is the massive deposition of BIFs from the seawater column\u0026nbsp;through\u0026nbsp;extensive Fe(II)\u003csub\u003eaq\u003c/sub\u003e oxidation\u0026nbsp;during the early\u0026nbsp;Precambrian (dominantly during 3.8-1.8 Ga)\u003csup\u003e6\u003c/sup\u003e. The geochemical, isotopic and mineralogical records of BIFs\u0026nbsp;exhibit\u0026nbsp;temporal and spatial variations. For example, the average valence state of Fe in BIFs gradually increased over time, because of a\u0026nbsp;shift in dominant Fe minerals from magnetite (especially \u0026gt;2.9 Ga) to hematite (particularly after the Neoarchean)\u003csup\u003e7\u003c/sup\u003e, suggesting that Fe(II) oxidation process evolved. Currently\u0026nbsp;photo- and/or O\u003csub\u003e2\u003c/sub\u003e-dependent Fe(II) oxidation in the shallow euphotic zone of paleo-oceans is widely considered to account for BIF precipitation, but this model is difficult to explain the intriguing mineralogical or \u0026nbsp;geochemical changes of BIFs over time\u003csup\u003e8\u003c/sup\u003e. How the evolving biogeochemical processes affect Fe(II) oxidation pathways and the resulting mineral products across anoxic-oxic transition was rarely considered in the previous models.\u003c/p\u003e\n\u003cp\u003eThe early anoxic ocean (\u0026gt; 3.0 Ga) was filled with ammonium-replete ferruginous waters, where the main anaerobic biological processes included N\u003csub\u003e2\u003c/sub\u003e reduction to NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e and Fe(II)-based anoxic photosynthesis (photoferrotrophy) \u003csup\u003e9, 10\u003c/sup\u003e. At this time, vertical profiles of NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e and Fe(II) in paleo-oceans were uniform (Fig. 1a). As oxygenic photosynthesis emerged to gradually consume reductants\u003csup\u003e11\u003c/sup\u003e, the uniformly reducing water column evolved into a heterogeneous one due to the developments of redoxcline and chemocline (Fig. 1b)\u003csup\u003e12, 13\u003c/sup\u003e. These developments would have greatly changed the pathways of Fe(II) oxidation\u003csup\u003e14\u003c/sup\u003e. Under the rising redox state of the paleo-oceans, NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e would be continuously oxidized to nitrogen oxyanions (NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e, mainly NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e and NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e) even in anoxic waters\u003csup\u003e15, 16\u003c/sup\u003e that can be dated back at least to the Mesoarchean\u003csup\u003e12, 17\u003c/sup\u003e. As a result, an intermediate \u0026nbsp;nitrogenous zone\u0026nbsp;gradually developed between the upper oxidizing surface water and the lower\u0026nbsp;ferruginous water (Fig. 1b)\u003csup\u003e18, 19\u003c/sup\u003e. This\u0026nbsp;nitrogenous zone is\u0026nbsp;commonly found in\u0026nbsp;oxygen minimum zone (OMZ) of modern oceans and ferruginous lakes, both regarded as the analogues of the hypoxic Precambrian ocean\u003csup\u003e20, 21\u003c/sup\u003e. This nitrogenous layer is crucial to Fe(II) oxidation because it would act as a redoxcline/chemocline barrier by consuming O\u003csub\u003e2\u003c/sub\u003e and CO\u003csub\u003e2\u003c/sub\u003e from above via nitrification and by oxidizing the upwelling Fe(II)\u003csub\u003eaq\u003c/sub\u003e from below via N-dependent Fe(II) oxidation (general reaction: Fe(II) + NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e \u0026rarr; Fe(III) + N\u003csub\u003e2\u003c/sub\u003e)\u003csup\u003e22, 23\u003c/sup\u003e. The N-dependent Fe(II) oxidation mechanism would greatly decrease the dominance of the traditional photo- and/or O\u003csub\u003e2\u003c/sub\u003e-dependent Fe(II) oxidation by spatially separating\u0026nbsp;the\u0026nbsp;reactants required in previously proposed Fe(II) oxidation mechanisms (Fig. 1b)\u003csup\u003e8\u003c/sup\u003e.\u0026nbsp;Interestingly, the peak deposition of BIFs at 2.7-2.4 Ga, after the onset of aerobic nitrification (and the presence of nitrogenous layer)\u003csup\u003e24\u003c/sup\u003e but before the remarkable rise of atmospheric O\u003csub\u003e2\u003c/sub\u003e marked as the Great Oxygenation Event (GOE, 2.4-2.2 Ga)\u003csup\u003e25, 26\u003c/sup\u003e, argues for the potential importance of coupled N-Fe redox cycling to BIF deposition. However, direct evidence is lacking. Here we hypothesize that an active, biologically-driven N-Fe redox process develops around the nitrogenous layer in the shallow water (Fig. 1) that is responsible for Fe(II) oxidation and substantially contributes to BIF formation. To test this hypothesis, we investigated how the evolution of coupled processes of Fe(II) oxidation and N redox cycling affect the formation of BIF-related mineral products under the simulated Precambrian ocean conditions.\u003c/p\u003e"},{"header":"Response of nitrification and denitrification to temperature cooling","content":"\u003cp\u003eAmmonia, formed abiotically on early Earth (e.g., volcanic, lightning, bolide\u003csup\u003e\u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e30\u003c/span\u003e, \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e31\u003c/span\u003e\u003c/sup\u003e, serpentinization of ultrabasic rocks\u003csup\u003e\u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e32\u003c/span\u003e\u003c/sup\u003e) and biotically at later times\u003csup\u003e\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e\u003c/sup\u003e, was the predominant form of fixed N pool in the early reducing ocean (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003ea)\u003csup\u003e\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e, \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e33\u003c/span\u003e\u003c/sup\u003e. Aerobic ammonia oxidation, which can occur under extremely low oxygen level (at nM level)\u003csup\u003e\u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e34\u003c/span\u003e\u003c/sup\u003e or even in anoxic waters\u003csup\u003e\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e\u003c/sup\u003e, was dated back to at least\u0026thinsp;~\u0026thinsp;3.0 Ga\u003csup\u003e\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e\u003c/sup\u003e and would have triggered the N redox processes by supplying NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e species to the ancient oceans (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eb), but it was scarcely considered by current biogeochemical models. For example, at a low O\u003csub\u003e2\u003c/sub\u003e level, the end products of the N redox processes were highly sensitive to temperature, probably via the effect of temperature on microbial functions and incomplete nitrification and denitrification processes in response to temperature changes.\u003c/p\u003e \u003cp\u003eTo simulate the N redox processes in a gradually cooling hypoxic Precambrian ocean, nitrifying and denitrifying microbial consortia were enriched from hot springs in Xizang and Yunnan Provinces, China, which span broad geochemical and temperature gradients (Fig. \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e, Table \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e and S2). The reason to use hot spring as an analog of Precambrian ocean was because key physicochemical properties in hot springs, such as low contents of oxygen and organic carbon, and high contents of Fe, N and Si, are similar to those of the paleo-oceans\u003csup\u003e\u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e35\u003c/span\u003e\u003c/sup\u003e. Furthermore, the microorganism-dominated community in hot springs, including many thermophilic ancestors, is a good analog of the simple biosphere on the early earth\u003csup\u003e\u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e36\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eNitrifying enrichments were first recovered from diverse hot springs ranging from 75 \u003csup\u003eo\u003c/sup\u003eC to 30 \u003csup\u003eo\u003c/sup\u003eC (Fig. \u003cspan refid=\"MOESM2\" class=\"InternalRef\"\u003eS2\u003c/span\u003e and S3). Interestingly, the dominant product of NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e oxidation gradually shifted from NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e to NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e in response to a temperature decrease, with a temperature cross-over at 60\u0026thinsp;\u0026minus;\u0026thinsp;50 \u003csup\u003eo\u003c/sup\u003eC (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003ea) regardless of the spring water geochemistry. Consistently, ammonia oxidizing archaea (AOA, performing NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e oxidation to NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e) were ubiquitous in the enrichments, with thermophilic \u003cem\u003eNitrosocaldales\u003c/em\u003e being dominant in higher temperature (\u0026gt;\u0026thinsp;40 \u003csup\u003eo\u003c/sup\u003eC) and \u003cem\u003eNitrososphaerales\u003c/em\u003e at lower temperature. Nitrite-oxidizing bacteria (NOB), mainly \u003cem\u003eNitrospirales\u003c/em\u003e, that can oxidize NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e/NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e to NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e were only revealed at lower temperature (\u0026lt;\u0026thinsp;40 \u003csup\u003eo\u003c/sup\u003eC, Fig. S3). This observation is consistent with previous studies in that AOA were detected at temperature up to 90 \u003csup\u003eo\u003c/sup\u003eC, but most NOB isolates, if not all, were active under 60 \u003csup\u003eo\u003c/sup\u003eC\u003csup\u003e\u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e37\u003c/span\u003e, \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e38\u003c/span\u003e, \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e39\u003c/span\u003e, \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e40\u003c/span\u003e\u003c/sup\u003e. Therefore, a transition of fixed N from NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e to NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e and then to NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e may have occurred as a result of cooling of the Precambrian ocean.\u003c/p\u003e \u003cp\u003eNO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e generated by nitrification may be reduced by canonical denitrification under reducing condition. Therefore, canonical denitrifying consortia under the same temperature gradient were enriched to explore the stability of produced NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e under different temperature conditions (Fig. S4 and S5). Interestingly, accumulation of NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e resulting from NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction significantly decreased with temperature cooling (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003eb), i.e., higher temperature favored production of NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e. This was well illustrated in one representative hot spring flow channel, in which denitrifying consortia stoichiometrically accumulated NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e from NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction at 65 \u003csup\u003eo\u003c/sup\u003eC, less at 55 \u003csup\u003eo\u003c/sup\u003eC, and undetectable at 50 \u003csup\u003eo\u003c/sup\u003eC (Fig. S5). The denitrifying consortia were dominated by \u003cem\u003eHydrogenobacter\u003c/em\u003e (more abundant at high temperature) and \u003cem\u003eThermus\u003c/em\u003e (Fig. S4), two types of common denitrifying bacteria in hydrothermal habitats\u003csup\u003e\u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e41\u003c/span\u003e, \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e42\u003c/span\u003e\u003c/sup\u003e. In fact, incomplete denitrification of NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e and accumulation of NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e were commonly observed in thermophilic cultivations\u003csup\u003e\u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e43\u003c/span\u003e, \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e44\u003c/span\u003e, \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e45\u003c/span\u003e\u003c/sup\u003e and oxygen-depleted waters\u003csup\u003e\u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e46\u003c/span\u003e\u003c/sup\u003e. Therefore, NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e accumulation from ammonia nitrification or nitrate reduction would be a substantial source of N species especially under elevated temperatures.\u003c/p\u003e \u003cp\u003eIn summary, an evolving N inventory would have developed in the hypoxic cooling Precambrian ocean. A NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e-dominant nitrogenous layer may gradually form in the shallow water by incomplete nitrification (NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e\u0026rarr;NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e) and denitrification (weak NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction), especially in the early high temperature (\u0026gt;\u0026thinsp;50\u0026ndash;60 \u003csup\u003eo\u003c/sup\u003eC) ocean. With the cooling of the ancient ocean, NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e was gradually produced in larger quantities through complete nitrification at lower temperature (especially\u0026thinsp;\u0026lt;\u0026thinsp;50 \u003csup\u003eo\u003c/sup\u003eC), leading to the pervasive mixture of NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e and NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e in the ocean, although an increasing proportion of NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e was also reduced into gaseous N species (e.g., N\u003csub\u003e2\u003c/sub\u003eO, N\u003csub\u003e2\u003c/sub\u003e) through denitrification.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e"},{"header":"Temperature-driven Fe(II) oxidation coupled with NO reduction","content":"\u003cp\u003eIn addition to production of NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e via nitrification and partial removal via denitrification, they can be reduced by an alternative and even more abundant electron donor in the ferruginous Precambrian ocean\u0026ndash;the rich Fe(II)\u003csup\u003e\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e, \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e27\u003c/span\u003e\u003c/sup\u003e. Fe(II) can be chemically oxidized by NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction (known as chemodenitrification) and/or microbially induced by NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction (known as nitrate-dependent Fe(II) oxidation, NDFO). Vertically, the NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e-rich layer just overlayed the lower Fe(II)-rich ferruginous water, providing an opportunity for chemo- and microbial denitrification. However, how NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e-dependent Fe(II) oxidation occurred under the scenario of the evolving NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e pool and cooling temperature are unclear. Therefore, chemical and biological induced NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e - dependent Fe(II) oxidation was simulated under a broad range of temperature schemes (25-75\u003csup\u003eo\u003c/sup\u003eC), with consideration of co-effects on mineral formation of HCO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e and dissolved Si that were rich in the Precambrian ocean\u003csup\u003e\u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e47\u003c/span\u003e,\u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e48\u003c/span\u003e, \u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e49\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eChemodenitrification was tested at temperatures ranging from 25 \u003csup\u003eo\u003c/sup\u003eC to 75 \u003csup\u003eo\u003c/sup\u003eC, which showed higher Fe(II) oxidation and NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction (both the rate and extent) by higher temperature (Fig. S6). Mineral formation also changed systematically with temperature cooling (summarized in Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). In the absence of dissolved Si, magnetite that can reach micrometer-scale size was the main or even only mineral product at temperature higher than 55 \u003csup\u003eo\u003c/sup\u003eC (Fig. S7, S9-a3, a4, b3, b4; Fig. S8-a, b). When HCO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e was present, magnetite started to form at 40 \u003csup\u003eo\u003c/sup\u003eC (Fig. S7, S9-b2; Fig. S8-a). In contrast, lepidocrocite and goethite predominantly precipitated at temperatures of 25 and 40 \u003csup\u003eo\u003c/sup\u003eC when supplemented with Cl\u003csup\u003e-\u003c/sup\u003e and HCO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e, respectively (Fig S7, S9-a1, a2, b1, b2). Addition of dissolved Si did not prevent Fe(II) oxidation by NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e but significantly altered the iron mineral phases and crystallization, as the main minerals turned to be weakly crystallized cronstedtite (empirical formula: Fe\u003csup\u003e2\u0026thinsp;+\u003c/sup\u003e\u0026thinsp;\u003csub\u003e\u003cem\u003e2\u003c/em\u003e\u003c/sub\u003eFe\u003csup\u003e3\u0026thinsp;+\u003c/sup\u003e\u0026thinsp;\u003csub\u003e\u003cem\u003e2\u003c/em\u003e\u003c/sub\u003eSiO\u003csub\u003e5\u003c/sub\u003e(OH)\u003csub\u003e4\u003c/sub\u003e, an Fe(III)-containing greenalite-like serpentine) and greenalite while a small part of magnetite only existed at higher temperature (Fig. S7, S8, S9-c).\u003c/p\u003e \u003cp\u003eBiologically induced NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e - dependent Fe(II) oxidation was first tested with the use of a typical thermophilic NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e-reducing isolate from a Xizang hot spring, \u003cem\u003eThermus\u003c/em\u003e sp., at 55 \u003csup\u003eo\u003c/sup\u003eC and 75 \u003csup\u003eo\u003c/sup\u003eC. Fe(II) was effectively oxidized by NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction at both temperatures, regardless of the presence of Si (Fig. S10). NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e was accumulated from NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction without Fe(II) (Fig. S10a), but it was not observed in the presence of Fe(II) (Fig. S10-c, d), suggesting that Fe(II) oxidation either consumed the produced NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e or bypassed it during the NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction pathway. Magnetite was the only mineral product at both temperatures without Si (Fig. S11-a1, a2). When Si was present, cronstedtite was the dominant well-crystalline mineral at 55 \u003csup\u003eo\u003c/sup\u003eC (Fig. S11-b1), accompanied with some greenalite (Fig. S8-d). Magnetite was co-precipitated with cronstedtite and greenalite at 75 \u003csup\u003eo\u003c/sup\u003eC (Fig. S11-b2, Fig. S8-e). Notably, microbially formed silicate minerals in Si-amended treatment were more crystalline compared to those formed by chemodenitrification (compared Figs. S11-b and S7-c). Many of these minerals tightly encrusted the cell surface (Fig. S12), suggesting that microbial activity greatly stimulated mineral crystallization.\u003c/p\u003e \u003cp\u003eThree representative denitrification consortia, enriched from a spring channel (Fig. \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e-b1) of different temperatures but similar water chemistry, were tested for their performance in Fe(II) oxidation. The three consortia were dominated by \u003cem\u003eHydrogenobacter\u003c/em\u003e sp. at high temperature (65 \u003csup\u003eo\u003c/sup\u003eC) and by \u003cem\u003eThermus\u003c/em\u003e sp. at lower temperature (55 and 50 \u003csup\u003eo\u003c/sup\u003eC, Fig, S4). Fe(II) oxidation occurred in consortia at higher temperature (\u0026gt;\u0026thinsp;50 \u003csup\u003eo\u003c/sup\u003eC) when NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e was produced as a byproduct of NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction (Fig. \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e3-b, c), but did not occur without consortia or in consortia of lower-temperature (50 \u003csup\u003eo\u003c/sup\u003eC) (Fig. \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e3-a), suggesting that Fe(II) was oxidized metabolically and/or chemically by NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e. The mixture of cronstedtite and magnetite was the main mineral products (Fig. \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e1-c), similar to that formed by pure \u003cem\u003eThermus\u003c/em\u003e sp. strain in the presence of Si, probably due to the fact that the hot spring water contained a considerable amount of Si (Table \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e). Mineral particles, especially for the cronstedtite formed by the denitrifying consortia (Fig. \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e4), however, were larger in size than those formed by pure \u003cem\u003eThermus\u003c/em\u003e strain, perhaps due to slower Fe(II) oxidation rate or interspecies interaction in the microbiota.\u003c/p\u003e \u003cp\u003eIn summary, higher temperature (over ~\u0026thinsp;50 \u003csup\u003eo\u003c/sup\u003eC) favored the precipitation of Fe(II)-Fe(III)-mixed minerals, especially magnetite, either via chemical or biological Fe(II) oxidation when coupled with NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction; in comparison, lower temperature was more beneficial to the formation of Fe(III) minerals (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). This variation in mineralogy in response to a temperature gradient is consistent with the trend observed in natural BIFs, that is, early BIFs (at higher temperature) were dominated by magnetite, and later (at lower temperature) gradually shifted to hematite (as partially summarized in Table S3). In addition, the presence of denitrifying microbial consortia tends to promote the formation of magnetite at lower temperature, with a higher proportion and better crystallinity relative to their absence, suggesting the importance of direct (mediate N-Fe reactions) and indirect (such as providing mineral adsorption sites for crystallization) biological effects on iron mineral precipitation in BIFs.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eIron minerals precipitated by chemical and biological N-Fe redox coupling under temperature gradient \u003csup\u003e\u003cb\u003ea\u003c/b\u003e\u003c/sup\u003e\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"6\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eTemperature\u003c/p\u003e \u003cp\u003e(\u003csup\u003eo\u003c/sup\u003eC)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eReactions\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colspan=\"4\" nameend=\"c6\" namest=\"c3\"\u003e \u003cp\u003eIron minerals\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eLepidocrocite\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eGoethite\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eMagnetite\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003eSilicates\u003c/p\u003e \u003cp\u003e(Cronstedtite, Greenalite)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u0026lt;\u0026thinsp;40\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eChemodenitrification\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cb\u003e+ +\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e+ +\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cb\u003e-\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u003cb\u003e+ + +?\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eMicrobial NDFO\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cb\u003e/\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e/\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cb\u003e/\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u003cb\u003e/\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e40\u0026ndash;55\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eChemodenitrification\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cb\u003e+ +\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e+ +\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cb\u003e+ +\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u003cb\u003e+ + +\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eMicrobial NDFO\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cb\u003e-\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e-\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cb\u003e+ + +\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u003cb\u003e+ + +\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u0026gt; 55\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eChemodenitrification\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cb\u003e-\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e+\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cb\u003e+ + +\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u003cb\u003e+ + +\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eMicrobial NDFO\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cb\u003e-\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e-\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cb\u003e+ + +\u003c/b\u003e\u003c/p\u003e \u003cp\u003e\u003cb\u003e+ +\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u003cb\u003e+ +\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003e \u003csup\u003e \u003cb\u003ea\u003c/b\u003e \u003c/sup\u003e Summarized based on the mineral composition in Figs. S7-S9, S11, S12, S14. More signs of \u0026ldquo;+\u0026rdquo; denote higher abundance. Black \u0026ldquo;+\u0026rdquo; symbols show the mineral composition in Si-absent treatments, while red \u0026ldquo;+\u0026rdquo; symbols show that in Si-rich systems; \u0026ldquo;-\u0026rdquo; denotes not detectable, and \u0026ldquo;/\u0026rdquo; denotes not tested in this study.\u003c/p\u003e"},{"header":"Coupled N-Fe redox cycles for the mineralogical succession of BIFs","content":"\u003cp\u003eReconstruction of the effect of biogeochemical evolution on BIF across geological timescale is extremely difficult due to the uncertainty of changes in key environmental factors. For example, oxygen level is a crucial factor determining whether Fe(II) oxidation is influenced by oxic or anoxic processes. However, it is difficult to determine the evolution of oxygen level in paleo-oceans with heterogeneous chemical structures, despite the widespread consensus of an overall rise of oxygen in the atmosphere of the early Earth. In comparison, temperature cooling is more predictable. From a long-term geological perspective, temperature cooling of the paleo-oceans is an indisputable fact, although the absolute magnitude of cooling is still controversial. Nevertheless, the cooling trend of temperature of the Archean-Proterozoic oceans would greatly reshape the structure and functional composition of microbial communities, thereby altering biogeochemical processes in the ocean, including the N and Fe cycling and BIF deposition. In the present work, by integrating all the results, we developed a four-stage evolution scenario for the coupled N-Fe redox processes, providing a possible explanation for the secular changes of iron mineral precipitation in BIFs in the Archean-Paleoproterozoic ocean (Fig.\u0026nbsp;4):\u003c/p\u003e \u003cp\u003eSmall scale BIFs (i.e., with typical laminated Si-rich and Fe-rich layers) began to deposit as early as 3.8 Ga. ago.\u003csup\u003e\u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e50\u003c/span\u003e\u003c/sup\u003e The ocean was hot (most probably higher than 55 \u003csup\u003eo\u003c/sup\u003eC, even over 75 \u003csup\u003eo\u003c/sup\u003eC)\u003csup\u003e\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e, \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e47\u003c/span\u003e, \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e51\u003c/span\u003e\u003c/sup\u003e, highly reducing, and almost devoid of any microbial activity (if any). Iron minerals in these oldest BIFs are overwhelmingly dominated by magnetite, accompanied by some Fe-silicates, such as grunerite, but few contain hematite\u003csup\u003e\u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e52\u003c/span\u003e\u003c/sup\u003e. During this prebiotic era, abiotic N\u003csub\u003e2\u003c/sub\u003e fixation was the main process of introducing a low flux of fixed N, (initially NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e ) (~\u0026thinsp;10\u003csup\u003e6\u003c/sup\u003e-10\u003csup\u003e10\u003c/sup\u003e mol N∙year\u003csup\u003e-1\u003c/sup\u003e or even higher), into the ferruginous ocean\u003csup\u003e\u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e30\u003c/span\u003e, \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e53\u003c/span\u003e\u003c/sup\u003e. The NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e would be rapidly reduced through chemical oxidation of Fe(II) especially at high temperature, followed by precipitation of iron in the form of magnetite (2NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e + 9Fe\u003csup\u003e2+\u003c/sup\u003e + 16HCO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e\u0026rarr;N\u003csub\u003e2\u003c/sub\u003e\u0026thinsp;+\u0026thinsp;3Fe\u003csub\u003e3\u003c/sub\u003eO\u003csub\u003e4\u003c/sub\u003e\u0026thinsp;+\u0026thinsp;8H\u003csub\u003e2\u003c/sub\u003eO\u0026thinsp;+\u0026thinsp;16CO\u003csub\u003e2\u003c/sub\u003e, as shown in Fig. S6-c), and/or cronstedtite in the presence of Si. Therefore, although NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e would not be accumulated to a considerable concentration, its abiotic supply was sufficient to precipitate a large proportion of the oldest BIFs (totally\u0026thinsp;~\u0026thinsp;10\u003csup\u003e11\u003c/sup\u003e-10\u003csup\u003e12\u003c/sup\u003e mol Fe in the Paleoarchean BIFs estimated by the BIF deposit size and average 20 wt% Fe content, Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ea). Moreover, the primary production of Fe(II)-Fe(III)-mixed minerals (magnetite, silicates) eases the vexatious requirement of a reduction step of ferric iron precursors (e.g., ferrihydrites), as proposed previously\u003csup\u003e\u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e54\u003c/span\u003e\u003c/sup\u003e. This scenario offers a reasonable explanation for the higher abundance of magnetite in the early BIFs\u003csup\u003e\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eAfter the Mesoarchean, deposition of BIFs increased slightly, until the Neoarchean. Magnetite is still the predominant iron mineral in most BIFs (particularly\u0026thinsp;\u0026gt;\u0026thinsp;2.9 Ga)\u003csup\u003e\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e\u003c/sup\u003e. During the Mesoarchean, biological N\u003csub\u003e2\u003c/sub\u003e fixation bloomed and greatly enlarged the NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e flux to the ocean\u003csup\u003e\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e, \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e\u003c/sup\u003e. Microbial oxidation of NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e may also emerge as early as in the Mesoarchean\u003csup\u003e\u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e55\u003c/span\u003e\u003c/sup\u003e, as AOA could have oxidized ammonia at extremely low levels of O\u003csub\u003e2\u003c/sub\u003e or even in the anoxic water \u003csup\u003e\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e, \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e\u003c/sup\u003e. Moreover, local \u0026ldquo;oxygen oasis\u0026rdquo;, due to the emerging oxygenic photosynthesis\u003csup\u003e\u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e55\u003c/span\u003e\u003c/sup\u003e, may have gradually stimulated NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e oxidation\u003csup\u003e12\u003c/sup\u003e. Therefore, microbial nitrification provided additional NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e flow, mainly NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e, as the temperature was still likely much higher than modern oceans (over 50 \u003csup\u003eo\u003c/sup\u003eC, as indicated in Figs.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003ea and 4). With the increase of NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e flux, chemical oxidation of Fe(II) by NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e, which primarily forms magnetite and cronstedtite, was still the predominant process of coupled N-Fe processes. This scenario offers an explanation for the increase of magnetite-dominant BIFs volume (totally\u0026thinsp;~\u0026thinsp;10\u003csup\u003e14\u003c/sup\u003e-10\u003csup\u003e15\u003c/sup\u003e mol Fe in Mesoarchean BIFs as estimated by the BIFs deposit size and average 20 wt% Fe content, Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003eb)\u003csup\u003e\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eBIF deposition increased significantly after the Neoarchean, reaching a peak from the mid-Neoarchean to the early Paleoproterozoic (2.7\u0026ndash;2.4 Ga), right before GOE. Intriguingly, hematite content increased dramatically in these BIFs, especially after 2.6 Ga, suggesting that certain important transition of biogeochemical processes might have occurred and significantly affected the Fe redox cycle. Indeed, the oxygenation of surface water was more pervasive at this time, which greatly stimulated aerobic nitrification and further increased the NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e flux. For example, the extremely positive excursions in δ\u003csup\u003e\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e\u003c/sup\u003eN was observed in the 2.7\u0026ndash;2.5 Ga sediments, which was interpreted as a great rise in N loss via coupled nitrification-denitrification processes\u003csup\u003e\u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e56\u003c/span\u003e, \u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e57\u003c/span\u003e\u003c/sup\u003e. Therefore, the abundant NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e might be extensively reduced by Fe(II) oxidation considering the super-large BIF deposition during this period. However, as temperature continued to decrease (lower than 50 \u003csup\u003eo\u003c/sup\u003eC), microbial nitrification of NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e would produce a mixture of NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e and NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e with an increasing share of NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e. With the increased NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e pool/flux, Fe(II) oxidation coupled with microbial NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction and chemical NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction produced a mineral assemblage of magnetite, silicates, and Fe(III) hydroxides (i.e., goethite, lepidocrocite, Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ec). Over time at certain temperature and pressure, these ferric hydroxides can transform to hematite\u003csup\u003e\u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e58\u003c/span\u003e\u003c/sup\u003e. Furthermore, the relative dominance of Fe(III) hydroxides produced by N-Fe redox coupling would gradually increase at lower temperatures (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e), which offers a plausible explanation for the transition of magnetite-dominant to hematite-dominant BIFs during this period.\u003c/p\u003e \u003cp\u003eA dramatic decrease or even stop of BIF deposition was observed after 1.8 Ga when the temperature further cooled down, suggesting a quiescence of Fe(II) oxidation at this time (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ed). Two possible reasons may account for this transition. First, canonical nitrification-denitrification cycles might outcompete the coupled N-Fe cycles, due to rapid and complete oxidation of NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e (into NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e) and complete reduction of NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e to N\u003csub\u003e2\u003c/sub\u003eO and N\u003csub\u003e2\u003c/sub\u003e gases (Fig. \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003ed, S4c) at low temperatures. Second, the development of an euxinic zone (S\u003csup\u003e\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e-\u003c/sup\u003e rich layer, caused by increased sulfate input from oxidative weathering of continental sulfides) between the nitrogenous and ferruginous layers provided an important reductant (i.e., S\u003csup\u003e\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e-\u003c/sup\u003e) to consume NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e and/or precipitate Fe(II)\u003csup\u003e\u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e59\u003c/span\u003e\u003c/sup\u003e, both of which would weaken the coupling of the N-Fe cycles. This scenario offers a possible explanation for the extremely low BIFs during the Meso- and Neoproterozoic (without considering the Rapitan IFs deposited during the Neoproterozoic).\u003c/p\u003e \u003cp\u003eIn summary, our proposed evolution model of the coupled N-Fe cycling processes, as a response to temperature decrease, provides a reasonable explanation for the successive change of abundance and mineralogy of BIFs. An important reason for the overlooked role of the coupled N-Fe cycles in the BIF formation in most previous studies is the assumption of the low accumulation of oxidative NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e species in the reducing Precambrian ocean. However, we argue that the increasing flux and changing speciation of NO\u003csub\u003ex\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e are extremely important for triggering extensive Fe(II) oxidation and mineral formation. A recent study found that the networked N-Fe reactions would provide substantial N\u003csub\u003e2\u003c/sub\u003eO emission and N burial (by association with Fe minerals) in the Precambrian marine ecosystem\u003csup\u003e\u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e60\u003c/span\u003e\u003c/sup\u003e, supporting the pervasive N-Fe reactions. Here we further demonstrated that N and Fe cycles could also be directly coupled to affect Fe mineralogy. In addition, our observed iron mineral assemblages formed by the dynamically evolving N-Fe coupling also have some other under-appreciated geological and environmental consequences, such as the bioavailability of N (via change of N speciation) and P (via adsorption to iron minerals) overtime, thereby controlling primary productivity and emission of greenhouse gasses N\u003csub\u003e2\u003c/sub\u003eO and CO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e60\u003c/sup\u003e. Finally, further work is required for additional assessment of the contribution of N-Fe coupling to BIF deposition, which include, but not limited to, the competition by different Fe(II) oxidation pathways, quantitative impacts of other evolutionary factors (e.g., pH, Ca/Mg), and the N and Fe isotopic footprints recorded in geological archives in response to temperature gradients.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e"},{"header":"Methods","content":"\u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003eThermophilic nitrification and denitrification consortia enrichment and analyses\u003c/h2\u003e \u003cp\u003eHot springs in the geothermal fields in Tengchong, Yunnan Province (Rehai, Ruidian and Houqiao), China, with diverse temperature and geochemical gradients, were sampled in September 2019, August 2020 and November 2021. Xizang (Dagejia, Quzhuomu and Qucai) hot springs were sampled in August 2020 (detailed in the Supplemental text, Fig. \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e, Tables S1 and S2). Thermophilic nitrifying and denitrifying consortia were preliminarily enriched in the field. At each selected hot spring, spring water mixed with sediment suspension was aseptically injected into pre-autoclaved Balch glass bottles with needles, which served as medium and microbial inoculant. The bottles were filled with air for nitrification enrichment but degassed by N\u003csub\u003e2\u003c/sub\u003e gas for denitrification enrichment. The main reason for using hot spring water as a medium was to minimize any bias caused by defined media. However, enrichment was also performed with defined media\u003csup\u003e\u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e61\u003c/span\u003e\u003c/sup\u003e in representative hot springs to test the stability of nitrification and denitrification. NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e and NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e (final concentrations 0.5-1 mM) were amended as substrates for nitrifying and denitrifying cultures, respectively, and the bottles were incubated in situ for 3\u0026ndash;5 days in hot springs to stimulate microbial growth. The \u003cem\u003ein-situ\u003c/em\u003e enrichments were subsequently transported to laboratory at ambient temperature in less than a week. In the lab the enrichments were incubated in incubators with temperatures similar to the corresponding springs. The concentrations of NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e, NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e and NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e were periodically monitored by spectrophotometric methods. The positive cultures that showed NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e oxidation or NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction were then transferred to new media. Transfer continued for 2\u0026ndash;5 times to obtain stable nitrification and denitrification consortia. Microbial compositions in successful enrichments were analyzed for representative temperatures (75 \u003csup\u003eo\u003c/sup\u003eC, 65 \u003csup\u003eo\u003c/sup\u003eC, 55 \u003csup\u003eo\u003c/sup\u003eC and 40 \u003csup\u003eo\u003c/sup\u003eC) by using the 16S rRNA gene pyrosequencing approach. Microbial and chemical analyses are provided in the SI.\u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003eFe(II) oxidation coupled with NO reduction (chemodenitrification)\u003c/h3\u003e\n\u003cp\u003eFe(II) oxidation by NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction (NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e + Fe\u003csup\u003e2+\u003c/sup\u003e \u0026rarr; N\u003csub\u003e2\u003c/sub\u003e\u0026thinsp;+\u0026thinsp;Fe\u003csup\u003e3+\u003c/sup\u003e) is also known as chemodenitrification. To mimic iron mineral formation by chemodenitrification under conditions of cooling and water chemistry rich in HCO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e and dissolved Si of the Precambrian ocean, four experimental sets were established at the temperature range of 25\u0026ndash;75 \u003csup\u003eo\u003c/sup\u003eC (as listed in Table S4) with and without Si (2 mM\u003csup\u003e\u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e48\u003c/span\u003e\u003c/sup\u003e). The reaction was buffered in PIPEs buffer to maintain the pH at 7, and the levels of Fe(II) (1 mM) and NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e (0.2 mM) were selected to simulate their low concentrations in the Precambrian ocean and ensure enough mineral formation for analysis. The medium was degassed with pure N\u003csub\u003e2\u003c/sub\u003e gas on a gassing station, autoclaved, and sampled in an anaerobic glove box. Fe(II) and NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e levels were regularly monitored and the final mineral products were collected for X-ray diffraction, scanning electronic microscopy, and M\u0026ouml;ssbauer analyses as detailed in the SI.\u003c/p\u003e \u003cp\u003e \u003cb\u003eFe(II) oxidation coupled with NO\u003c/b\u003e \u003csub\u003e \u003cb\u003e3\u003c/b\u003e \u003c/sub\u003e \u003csup\u003e \u003cb\u003e-\u003c/b\u003e \u003c/sup\u003e \u003cb\u003ereduction by\u003c/b\u003e \u003cb\u003eThermus\u003c/b\u003e \u003cb\u003esp.\u003c/b\u003e\u003c/p\u003e \u003cp\u003eMicrobial Fe(II) oxidation coupled with NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e reduction (NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e + Fe\u003csup\u003e2+\u003c/sup\u003e \u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\(\\underrightarrow{\\varvec{c}\\varvec{e}\\varvec{l}\\varvec{l}}\\)\u003c/span\u003e\u003c/span\u003e N\u003csub\u003e2\u003c/sub\u003e/N\u003csub\u003e2\u003c/sub\u003eO/NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e + Fe\u003csup\u003e3+\u003c/sup\u003e) is common among denitrifying bacteria\u003csup\u003e\u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e62\u003c/span\u003e\u003c/sup\u003e. A typical thermophilic denitrifier, \u003cem\u003eThermus\u003c/em\u003e sp. isolated from Tibet hot spring (DGJ, 70 \u003csup\u003eo\u003c/sup\u003eC) and having a broad range of growth temperature (50\u0026ndash;80 \u003csup\u003eo\u003c/sup\u003eC, optimal 60 \u003csup\u003eo\u003c/sup\u003eC), was used to test its capability of Fe(II) oxidation. \u003cem\u003eThermus\u003c/em\u003e sp. was grown in T5 medium (Table S5), which was then washed three times by 10 mM PIPEs buffer to remove any organic substrates. The collected \u003cem\u003eThermus\u003c/em\u003e sp. cells were used for NDFO test in a final concentration of ~\u0026thinsp;1\u0026times;10\u003csup\u003e7\u003c/sup\u003e cells per mL. The PIPES-buffered non-growth medium, the same as that for chemodenitrification, was used, with NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e replaced by NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e. Four experimental sets were established at two temperatures (55 \u003csup\u003eo\u003c/sup\u003eC and 75 \u003csup\u003eo\u003c/sup\u003eC) to compare the effects of cells and silica on mineral formation (Table S5).\u003c/p\u003e\n\u003ch3\u003eFe(II) oxidation coupled with NO reduction by denitrifying consortia\u003c/h3\u003e\n\u003cp\u003eThree canonical denitrifying enrichment consortia from the same hot spring stream with different temperatures (DG1-1, DG1-2 and DG1-3 at 65, 60 and 50 \u003csup\u003eo\u003c/sup\u003eC, respectively, Fig. \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e) were selected to test their potential capability on Fe(II) oxidation and mineral formation. The water collected from the source spring was used as the medium for all three consortia. Three experimental sets were established for each consortium to compare their effects on Fe(II) oxidation (Table S6): a) abiotic control without inoculation, b) Fe(II)\u0026thinsp;+\u0026thinsp;inoculated consortia to test any electron acceptor possibly present in the hot spring water itself, and c) NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e + Fe(II)\u0026thinsp;+\u0026thinsp;inoculated consortia.\u003c/p\u003e"},{"header":"Declarations","content":"\u003ch2\u003eCompeting interests\u003c/h2\u003e \u003cp\u003eThe authors declare no competing interests.\u003c/p\u003e \u003ch2\u003eAuthor contributions\u003c/h2\u003e \u003cp\u003eLH and YD contributed equally to conceptualization, data analysis and draft writing. LH, YD, LL, JY and LM performed data collection. LH, HJ and HD acquired fundings. LH, YD, HD and HJ wrote the original draft, and all authors reviewed and edited the manuscript.\u003c/p\u003e\u003ch2\u003eAcknowledgments\u003c/h2\u003e \u003cp\u003eThis work was supported by the National Natural Science Foundation of China (NSFC- 42192503, 42172340, 42192500, 91951205), and the \u0026ldquo;Deep-time Digital Earth\u0026rdquo; Science and Technology Leading Talents Team Funds for the Central Universities for the Frontiers Science Center for Deep-time Digital Earth, China University of Geosciences (Beijing) (Fundamental Research Funds for the Central Universities; grant number: 2652023001)\u0026rdquo;.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eMcGunnigle JP, Cano EJ, Sharp ZD, Muehlenbachs K, Cole D, Hardman MF, \u003cem\u003eet al.\u003c/em\u003e Triple oxygen isotope evidence for a hot Archean ocean. 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Nature Communications 2013, 4: 1533.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBuessecker S, Imanaka H, Ely T, Hu R, Romaniello SJ, Cadillo-Quiroz H. Mineral-catalysed formation of marine NO and N\u003csub\u003e2\u003c/sub\u003eO on the anoxic early Earth. Nature Geoscience 2022, 15(12): 1056\u0026ndash;1063.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBollmann A, French E, Laanbroek HJ. Chapter three - Isolation, Cultivation, and Characterization of Ammonia-Oxidizing Bacteria and Archaea Adapted to Low Ammonium Concentrations. In: Klotz MG (ed). \u003cem\u003eMethods in Enzymology\u003c/em\u003e, vol.\u0026nbsp;486. Academic Press, 2011, pp\u0026nbsp;55\u0026ndash;88.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eWeber KA, Achenbach LA, Coates JD. Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nature Reviews Microbiology 2006, 4(10): 752.\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":false,"hasPassedJournalQc":"","hasAnyPriority":true,"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":"nature-portfolio","isNatureJournal":true,"hasQc":false,"allowDirectSubmit":false,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"","title":"Nature Portfolio","twitterHandle":"","acdcEnabled":false,"dfaEnabled":false,"editorialSystem":"ejp","reportingPortfolio":"","inReviewEnabled":true,"inReviewRevisionsEnabled":false},"keywords":"","lastPublishedDoi":"10.21203/rs.3.rs-3724120/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3724120/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eBiogeochemical cycles in the Precambrian ocean responded to the co-evolution of biosphere (microorganisms) and the physicochemical structure (e.g., redox, temperature) of the ocean, which closely link to the enigma of banded iron formations (BIFs) that primarily triggered by massive Fe(II) oxidation under anoxic-hypoxic condition for two-billon years (~3.8-1.8 Ga). The current Fe(II) oxidation models, however, rarely consider the effects of the evolution of coupled biogeochemical cycles on secular succession (shifting from magnetite to hematite) of dominant iron minerals in BIFs. Here, we investigated the evolution of coupled Fe-N redox processes under the simulated Precambrian ocean conditions, and propose a dynamic model for the origin of iron mineral succession in BIFs: During the early-mid Archean, NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e was mainly produced by nitrification in the oceans of warm-hot temperatures (\u0026gt;50-60 \u003csup\u003eo\u003c/sup\u003eC), which favored the primary precipitation of Fe(II)-Fe(III) oxides (magnetite) and silicates (cronstedtite) in the early BIFs. Subsequently, the cooling and oxygenation of paleo-ocean near the GOE promoted the input of both NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e- \u003c/sup\u003eand NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e, resulting in co-precipitation of an increasing amount of Fe(III) minerals (goethite and lepidocrocite as precursors of hematite). This dynamic N-Fe coupling model explains the observed secular transition of iron mineral phases in BIF deposition.\u003c/p\u003e","manuscriptTitle":"Co-evolving N-Fe redox processes controlled iron minerals in banded iron formation","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-01-08 17:23:32","doi":"10.21203/rs.3.rs-3724120/v1","editorialEvents":[],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"nature-geoscience","isNatureJournal":true,"hasQc":false,"allowDirectSubmit":false,"externalIdentity":"ngeo","sideBox":"Learn more about [Nature Geoscience](http://www.nature.com/ngeo/)","snPcode":"","submissionUrl":"","title":"Nature Geoscience","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"ejp","reportingPortfolio":"Nature Research","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"e07e5fc4-987c-4851-8c13-28c4840fdde3","owner":[],"postedDate":"January 8th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"under-review","subjectAreas":[{"id":27206850,"name":"Earth and environmental sciences/Biogeochemistry/Element cycles"},{"id":27206851,"name":"Earth and environmental sciences/Planetary science/Mineralogy"}],"tags":[],"updatedAt":"2026-04-12T13:20:37+00:00","versionOfRecord":[],"versionCreatedAt":"2024-01-08 17:23:32","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-3724120","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3724120","identity":"rs-3724120","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}