Plate Tectonic History and Ocean Oxygenation Shaping Biogeography of Hydrothermal Bacterial Community

Plate Tectonic History and Ocean Oxygenation Shaping Biogeography of Hydrothermal Bacterial Community | 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 Plate Tectonic History and Ocean Oxygenation Shaping Biogeography of Hydrothermal Bacterial Community Weiguo Hou, Shang Wang, Hongyu Chen, Hanhui Liu, Yidi Zhang, Fangru Li, and 2 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-7588813/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Plate tectonics has fundamentally shaped the biogeography and evolution of macroscopic life, but its influence on microbial distributions remains poorly understood. Here, we demonstrate that the global biogeography of hydrothermal vent-endemic microbiota —specifically, lithoautotrophic bacterial families within the phyla Campylobacterota, Aquificota, and Thermosulfidibacterota (collectively CAT families) — is structured by tectonic history. CAT families, particularly obligate anaerobes, are significantly more abundant in early-origin Pacific, Arctic, and Mediterranean oceans, whereas they are notably scarce in late-formed Atlantic and Indian Oceans. We attribute this pattern to the timing of ocean formation and its interplay with global redox evolution. During the genesis of the former three oceans, anoxic conditions facilitated the unrestricted dispersal among oceans and colonization of anaerobic CAT families in hydrothermal vents. In contrast, fully oxygenated conditions during the formation of the two later oceans imposed a dual barrier: molecular oxygen was toxic to obligate anaerobes, and the oxidation of reduced chemicals depleted the energy sources necessary for facultative aerobes. Our findings established that plate tectonics has imposed first-order constraints on microbial biogeography through long-term modulation of ocean chemistry and habitat connectivity. These results integrate microbial dispersal into a geodynamic framework, revealing that even microbial life is subject to planetary-scale geological constraints. Earth and environmental sciences/Planetary science/Tectonics Earth and environmental sciences/Ecology/Biodiversity Earth and environmental sciences/Ocean sciences/Marine biology hydrothermal vents microbial community global distribution tectonic history ocean oxygenation Figures Figure 1 Figure 2 Figure 3 Figure 4 Main The determinants of geographic range size represent a central question in macroecology. Syntheses of studies across plants and animals confirm that dispersal ability is a foundational, albeit variable, predictor of species' distributions 1,2 . For microorganisms, however, the classic tenet that ‘everything is everywhere, but the environment selects’ has long implied that their immense population sizes and dispersal potential negate the influence of geographic barriers 3 . This paradigm is increasingly challenged by evidence of endemism in isolated habitats 4,5 6 , raising a critical question: can large-scale geological processes impose dispersal limitations sufficient to structure the global distribution of microorganisms? Hydrothermal vent systems, emerging along mid-ocean ridges and subduction-related back-arc basins, discharge reducing fluids rich in energy sources such as H₂, H₂S, CH₄, and reduced metals.These fluxes establish steep physico-chemical gradients that sustain prolific chemosynthetic ecosystems 7-9 . Among the key microbial colonists are members of the phyla Campylobacterota (formerly Epsilonproteobacteria), Aquificota, and Thermosulfidibacterota 10,11 . These taxa, collectively termed the CAT phyla, include anaerobic and microaerophilic lineages that are highly adapted to vent conditions 12-14 . Their ecological fidelity is profound: CAT abundances track vent activity, declining precipitously upon vent quenching 15-18 . Such strict habitat dependence and limited dispersal potential make the CAT phyla ideal model organisms for probing biogeographic controls in the deep sea. The distribution of vent habitats itself is a product of planetary-scale tectonic processes. Plate motions continuously create and destroy vent systems over millions of years 19 , while concurrent shifts in global ocean redox state 20 , especially the global oxygenation of the deep ocean 21,22 , fundamentally altered the biogeochemical context for anaerobic life 23 . Yet, the extent to which these deep-time geological events have imprinted the contemporary biogeography of vent microbiomes is entirely unknown. Here, we synthesize global microbial community data from deep-sea vents with paleo-oceanographic reconstructions to test the hypothesis that plate tectonics has shaped modern distributions of CAT lineages. We demonstrate that their biogeography is not random but reflects the timing of ocean basin formation and oxygenation, providing evidence that geological history mediates microbial dispersal and diversification across the oceans. A brief review of the tectonic and geochemical evolution history of the global oceans The Wilson Cycle posits that periodic opening and closing of ocean basins, driven by plate tectonics 19 , continuously generates and eliminates hydrothermal vent habitats. The modern Pacific Ocean initiated formation at ~190 million years ago (Ma) within the vast Panthalassic Ocean (the proto-Pacific Ocean) 24 , which itself originated from the breakup of Rodinia during the Neo-Proterozoic (around 700-600 Ma) 25 . The Mediterranean Sea represents a remnant of the Paleo-Tethys Ocean, which opened during the Neoproterozoic (around 650 Ma) 26-29 . The Arctic Ocean is bounded by continental shelves and cratonic blocks, including the Canadian Arctic Islands, Greenland, North American, the Barents Shelf, the Baltic Shield, and Siberian 30 . It comprises the Amerasia and Eurasia Basins, which formed at ~ 140 Ma and ~ 56 Ma, respectively 31,32 . Prior to the Arctic Ocean, the extinct South Anyui Ocean existed within the circum-Arctic region, which opened around 400 Ma 31,33,34 . In contrast, the Atlantic and Indian Oceans are comparatively young, having formed between ~ 195 Ma and 130 Ma following the breakup of the Pangaea super-continent 35-37 . The Red Sea—the youngest ocean hosting hydrothermal vents—initiated rifting ~25-30 Ma with the separation of the Arabian-Nubian Shield 38,39 . We therefore hypothesize that microbial communities in hydrothermal systems of the Pacific, Mediterranean, and Arctic Oceans were inherited from pre-existing oceanic systems, whereas those in the Atlantic, Indian, and Red Sea were colonized via dispersal from adjacent oceans. Since the Proterozoic, ocean chemistry has undergone dramatic changes as a result of oxygenation 40 . Before the Proterozoic Eon (4.0-2.5 billion years ago, Ga), the global oceans were pervasively anoxic. The Proterozoic (2.5-0.54 Ga) marked the onset of surface ocean oxygenation, followed by stepwise increases throughout the Phanerozoic (540 Ma), culminating in fully oxygenated deep oceans by the early Paleozoic (~440-420 Ma) 21 . This trend was episodically interrupted by Mesozoic oceanic anoxic events (OAEs; 183 to 85 Ma), each lasting ~1.5 Ma 41,42 . These redox shifts progressively transformed seawater from a reducing chemistry rich in Fe 2+ , H 2 S, H 2 , S 0 , CH 4 , through a stratified state with oxic surface and anoxic deep waters, to a fully oxygenated system dominated by O 2 , SO 4 2- , and NO 3 - 20,21 . Temporally, the Pacific Ocean, Arctic Ocean, and the Mediterranean Sea originated prior to full ocean oxygenation, whereas the Atlantic, Indian oceans, and the Red Sea opened after deep ocean oxygenation. This temporal dichotomy may provide a first-order control on the assembly and evolution of vent microbial communities through geologic time. The evolution of the energy metabolism of the CAT phyla Within the CAT phyla, Campylobacterota and Aquificota contain both anaerobic and facultatively aerobic vent-specific families 43 . An evolutionary relationship among the families within the CAT phyla was inferred from the topography of the 120-concatenated-protein phylogeny (Fig. S1). The energy metabolism capacities were inferred from the isolate descriptions (supplementary material Table S1 and references therein) and the existence of genes responsible for metabolisms of hydrogen-, sulfur-oxidization, and sulfur-, nitrate-, and oxygen-reduction in the metagenome-assembled genomes (MAGs) (supplementary material Fig. S2-S6). The Campylobacterota phylum diverged from the Aquificota-Thermosulfidibacterota phyla at around 4.1 Ga, with a similar evolutionary history of energy metabolisms (Fig. 1). From the early-diverged families to the late-diverged lineages, the energy metabolism pathways become increasingly complex. The earliest evolved families (i.e., Thermosulfidibacteraceae, Desulfurobacteriaceae, and Hippeaceae, formed at 2.08-2.85 Ga) only harnessed the elemental sulfur-reduction with hydrogen for chemoautolithotrophic energy metabolism, which is also inherited by the rest of the CAT families. Then, nitrate was used as an additional electron acceptor in the families of Nautiliaceae and Desulfurobacteriaceae (formed at around 1.6 Ga), with NH 3 as the reducing product. At around 1.0 Ga, aerobic families (including Nitratiruptoraceae, Hydrogenimonadaceae, Sulfurovaceae, Sulfurimonadaceae, Hydrogenothermaceae, and Aquificaceae) formed, accompanied by an increase of sulfur species as electron donors, such as sulfide and thiosulfate, and molecular O 2 as the electron acceptor. Synchronously, the reducing products of nitrate shifted from NH 3 to N 2 or N 2 O (Fig. 1). Global distribution pattern of the CAT families Microbial community compositions, based on 16S rRNA gene amplicon data at the family level, revealed a pronounced divergence in the abundance of CAT families between ancient and younger oceans. Linear discriminant analysis (LDA) confirmed that the relative abundances of CAT families were significantly higher in early-formed oceans (Pacific and Arctic Oceans, and Mediterranean Sea) compared to the late-formed systems (Atlantic and Indian Oceans, and Red Sea) (Supplementary material Figures S7-S16). This disparity was visually evident in abundance-projected global maps (Fig. 2), which showed Campylobacterota were ubiquitous and highly abundant (>50% relative abundance) across most sampling sites, except in the Indian Ocean, South Atlantic Ocean, and Red Sea (Fig. 2a). Aquificota were prevalent (> 10% relative abundance) in the Pacific and Arctic Oceans, and Mediterranean Sea, while Thermosulfidibacterota occurred at lower abundances (> 1%), peaking in the Arctic Ocean near 10%. Obligately anaerobic lineages (Thermosulfidibacterota, Desulfurobacteriaceae, Nautiliaceae, Hippeaceae, and Desulfurellaceae) exhibited highly restricted distributions, with Desulfurobacteriaceae concentrated in the eastern Pacific, Hippeaceae and Desulfurellaceae largely confined to the Gulf of California (Fig. 2b). Notably, no anaerobic CAT members were detected in the Indian or South Atlantic Oceans. In contrast, facultatively aerobic families (Sulfurovaceae, Sulfurimonadaceae, Nitratiruptoraceae, Aquificae, and Hydrogenothermaceae) showed broader distributions (Fig. 2c), consistent with their respective phyla (Fig. 2a). Among them, Sulfurimonadaceae and Sulfurovaceae were the most abundant CAT families globally (Fig. 2d). Alpha diversity analyses further revealed systematic differences in the richness and phylogenetic diversity of CAT taxa across oceans. Hydrothermal vent systems in the Pacific Ocean exhibited the highest species richness (SR) and phylogenetic diversity (PD) for all three CAT phyla (Fig. 3). Campylobacterota (Fig. 3a&d) and Aquificota (Fig. 3b&e) showed significantly greater SR and PD in the Pacific compared to all other regions. Thermosulfidibacterota diversity was also highest in the Pacific, comparable to the Arctic Ocean (Fig. 3c&g). In contrast, the late-formed oceans—the Atlantic, Indian, and Red Sea—consistently hosted relatively lower CAT diversity (Fig. 3). Across all regions, taxonomic richness declined in the order: Campylobacterota > Aquificota > Thermosulfidibacterota. Together, these results demonstrate a clear biogeographic imprint of ocean basin ages on the diversity and distribution of hydrothermal vent microbiomes. The mechanism of the uneven distribution of the CAT families in the oceans The assembly of microbial communities is governed by both deterministic (niche-based) and stochastic (dispersal-driven) processes 45,46 . To quantify their relative contributions to the biogeographic patterns of CAT families, we applied the dispersal–niche continuum index (DNCI) 47,48 , a metric derived from a permutation-based framework (PER-SIMPER) that uses taxon occurrence data to disentangle assembly mechanisms 48,49 . Consistently negative DNCI values indicated that dispersal limitation, rather than niche selection, was the dominant driver of community dissimilarity between the early-formed (Pacific, Arctic, and Mediterranean) and the late-formed (Atlantic, Indian, and Red Sea) oceans (Table 1, Supplementary material Fig. S17). This pattern held for pairwise comparisons between adjacent oceans (Table 1, Supplementary material Fig. S18-S26). LefSe analysis further identified both anaerobic and facultatively aerobic CAT families as key biomarkers differentiating vent communities worldwide (Table 1, Supplementary material Fig. S7-S16), supporting the inference that their limited dispersal capacity underlies large-scale biogeographic divergence. Table 1 DNCI values between pairwise groups of hydrothermal microbial communities Oceanic pair groups DNCI values S.DNCI CAT families with differential distribution Early-Late -9.865961 0.06405824 Aquificaceae, Sulfurovaceae, Sulfurimonadaceae, Nautiliaceae, Hydrogenothermaceae, Desulfurobacteriaceae, B14-G1, Hydrogenimonadaceae, Hippeaceae, Desulfurellaceae, Thermosulfidibacteraceae, and Nitratiruptoraceae Pacific-Arctic -8.6011656 0.11960298 Sulfurimonadaceae, Sulfurovaceae, Nautiliaceae, and Hydrogenothermaceae Pacific-Atlantic -52.6056211 0.08219519 Thermosulfidibacteraceae, Hydrogenothermaceae, Desulfurobacteriaceae, Aquificaceae, Desulfurellaceae, Nitratiruptoraceae, Hippeaceae, and B14-G1 Pacific-Indian -17.9522868 0.12904323 Sulfurimonadaceae, Nautiliaceae, Thermosulfidibacteraceae, Desulfurobacteriaceae, Nitratiruptoraceae, and Hippeaceae Pacific-Mediterranean -219.8926051 0.26002027 Sulfurovaceae, Sulfurimonadaceae, Nautiliaceae, Thermosulfidibacteraceae, Aquificaceae, Desulfurellaceae, Desulfurobacteriaceae, and Hippeaceae Mediterranean_Atlantic -40.1411662 0.07002511 Hydrogenothermaceae, Nitratiruptoraceae, Sulfurimonadaceae, and B14-G1; Nautiliaceae Mediterranean-Indian -100.2812506 0.77249686 Nitratiruptoraceae; Hydrogenimonadaceae and Nautiliaceae Arctic-Atlantic -9.7230757 0.31240003 Desulfurobacteraceae, Thermosulfidibacteraceae, and B14-G1 Indian-Atlantic -29.3061837 0.26081572 Hydrogenimonadaceae Indian-Red Sea -59.2821389 0.52192536 Sufurovaceae, Sulfurimonadaceae, Hydrogenothermaceae, and Aquificaceae The deep ocean is thought to have become fully oxygenated by the late Paleozoic (~420 Ma) 50,51 . Molecular oxygen is toxic to anaerobic microorganisms, damaging biomolecules via reactive oxygen species and oxidizing low-redox-potential metalloenzymes 52 . Consistent with this, anaerobic CAT lineages encode significantly fewer antioxidant enzymes in their MAGs than aerobic counterparts (Extended Data Fig. 1), indicating poor oxygen tolerance and constrained dispersal through oxic waters. This explains the near-absence of anaerobic CAT families in the younger Indian Ocean and Red Sea (Fig. 3c). Most anaerobic lineages are instead confined to the Pacific, Arctic, and Mediterranean Oceans (Fig. 2b), consistent with their origins predating deep-sea oxygenation 50,51 (Fig. 1). Theoretically, the fully oxygenated Atlantic should also exclude anaerobic taxa, yet we detected Nautiliaceae in the North Atlantic (Fig. 3c). We propose that Mesozoic oceanic anoxic events (OAEs) may have facilitated their dispersal into the Central Atlantic Ocean (Fig. 2b), which opened earlier than other parts of the Atlantic Ocean and remained connected to the Pacific Ocean 33,37 . Oxygenation also diminishes the availability of reduced compounds (e.g., H 2 , H 2 S, S 0 , SO 3 2- , S 2 O 3 2- ) that serve as energy sources for facultatively aerobic CAT families, likely limiting their dispersal even in the presence of oxygen. Indeed, low abundances of the facultatively aerobic Hydrogenothermaceae, Sulfurovaceae, and Sulfurimonadaceae were observed in the Central and Southwest Indian Ocean (Fig. 2c), and Nitratiruptoraceae was sparse in the Northwest Indian Ocean, South Atlantic Ocean, and Red Sea. Further support comes from the Loihi hydrothermal field (~400 ka) in the Pacific, where newly formed vents host low abundances of facultative aerobic CAT families 53 , highlighting their slow colonization under modern oxidizing conditions. Nevertheless, specific lineages such as Sulfurimonadaceae (mainly genus Sulfurimonas ) and Sulfurovaceae (mainly genus Sulfurovum ) can disperse via particle-rich hydrothermal plumes that contain micro-niches with reduced compounds, providing a mechanism for long-range dispersal in oxic waters 54-56 . Distribution of CAT taxa through Earth’s redox history The evolution trajectory of CAT lineages reflects major transitions in ocean redox chemistry, which can be divided into anoxic, intermediate, and oxic stages 20 . During the anoxic stage (prior to ~ 2.45 Ga), the global ocean was rich in reduced compounds such as Fe 2+ , H 2 , S 0 , H 2 S, and NH 4 + (Fig. 4a) 22,23 , resembling the chemical environment of contemporary hydrothermal vent fluids. High ocean temperatures (~65 - 80 o C) 57 were near the optimal growth temperature (OGT) for the early-evolved CAT lineages (Extended Data Fig. 2), implying that ancestral CAT taxa (such as Thermosulfidibacterota, Hippeaceae, and Desulfurellaceae) were likely ubiquitous in the open ocean rather than vent-restricted. The Great Oxygenation Event (GOE) marked the onset of an intermediate phase, oxidizing surface waters and driving the accumulation of NO 2 - , NO 3 - , and SO 4 2- from reduced precursors (e.g., NH 4 + , S 0 , and H 2 S), while simultaneously decreasing H 2 availability in the deep ocean (Fig. 4b) 22,23 . Episodic deep-ocean oxygenation 58,59 likely promoted metabolic diversification within CAT lineages, favoring taxa capable of utilizing a wider array of electron acceptors. Lineages relying exclusively on H₂ as a sole electron donor (e.g., Desulfurobacteriaceae, Hautiliaceae, and Hydrogenimonadaceae) became increasingly restricted to hydrothermal vents, where H₂ remained abundant. In contrast, sulfur-oxidizing CAT families continued to proliferate in broader marine settings due to the persistence of S⁰, H 2 S, and S 2 O 3 2 ⁻ in seawater. By the Phanerozoic (~0.54 Ga onward), full ocean oxygenation 40 dramatically reduced the pool of reduced chemicals in the open ocean (Fig. 4c). As a result, both anaerobic and facultatively aerobic CAT taxa became largely confined to hydrothermal vent systems, where reductants remained plentiful. The sharp redox gradients between oxidized seawater and reduced vent fluids sustained high energy availability, fueling diverse microbial ecosystems at modern vents. Thus, the progressive oxygenation of Earth’s oceans systematically narrowed the ecological niches of CAT lineages, transforming them from widespread marine taxa into specialists of hydrothermal systems. Summary We reveal a pronounced biogeographic disjunction between ancient oceans formed under anoxic conditions (Pacific, Arctic, Mediterranean) and younger, oxygen-rich basins (Atlantic and Indian). In this study, we demonstrate that the biogeography of hydrothermal vent-specific bacteria, notably the CAT phyla (Campylobacterota, Aquificota, and Thermsulfidibacterota), is fundamentally shaped by the tectonic and geochemical evolution of oceans. We show that early-formed oceans (Pacific, Arctic, and Mediterranean Oceans) host significantly higher diversity and abundance of CAT lineages, including numerous anaerobic groups. In contrast, late-formed oceans (Atlantic, Indian Oceans, and the Red Sea) contained fewer CAT taxa, predominantly comprising aerobic families. This distribution reflects the interplay between ocean formation age and Earth’s redox history. Specifically, the Pacific, Arctic, and Mediterranean Oceans originated during periods of widespread anoxia, facilitating the unrestricted dispersal and establishment of anaerobic vent microbes. Conversely, the Atlantic and Indian Oceans formed after deep-ocean oxygenation, which imposed a dual constraint: molecular oxygen limited the dispersal of anaerobic taxa, while the diminished availability of reduced chemical compounds reduced energy supplies even for aerobic vent specialists. Our findings directly link plate tectonic processes and planetary-scale geochemical transitions to the assembly and distribution of microbial life. By revealing how deep-time geological events structured contemporary microbial biogeography, this study establishes a new framework for understanding the origins and dispersal of life in Earth’s subsurface biosphere. Methods A total of 1,192 Metagenome-assembled genomes (MAGs) affiliated with the phyla Campylobacterota, Aquificota, and Thermosulfidibacterota were retrieved from the NCBI database with the “Download Genome Taxon” function in the dataset tool. The taxonomy of the MAGs was verified using the GTDB-tk v0.3.3 tool 60 . Non-hydrothermal vent-derived MAGs were excluded from further analysis. The qualities of all retrieved MAGs were evaluated with CheckM v1.2.2. Any MAGs with completeness > 0.5 and contamination < 0.1 were selected for subsequent analyses. After quality filtering, 923 MAGs were targeted for further analysis (see the Source Data 1). The optimal growth temperatures (OGTs) of the MAGs were predicted using the TOME software 61 . The phylogenetic relationship of the CAT families was inferred from the concatenated 120 marker genes of the MAGs, which were identified, concatenated, and aligned using the GTDB-tk v0.3.3 tool 60 . A Maximum Likelihood tree was constructed using MEGA-12 software with the Jones-Taylor-Thornton model substitution with a bootstrap value of 1000 62 . Open reading frames (ORFs) of the MAGs were predicted with Prodigal v2.6.3. The predicted ORFs were searched against the NCBI nr protein database (2019/07) and eggNOG database with the BLASTP algorithm (coverage of > 75%, e-values of < 1 × 10 − 20 ) to check their protein identities to the most closely related sequences using DIAMOND sequence aligner version 0.9.30.131 ( http://github.com/bbuchfink/diamond ). Then, the genes related to energy metabolism pathways, including nitrogen cycling 63 , sulfur cycling 64 , oxygen reductases 65 , and hydrogenases 66 , as well as the antioxidases in each MAG, were counted using a Linux searching tool grep . The types of oxygen-respiration enzymes and hydrogenases were also analyzed using DIAMOND by searching against the Heme-Copper Oxidases (HCOs) and Hydrogenase databases 65 , 66 . These targeted genes were also verified using the online Conserved Domain Search Service (CD Search) in the NCBI web ( https://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi ). The hydrothermal vent-related high-throughput 16S rRNA gene sequence datasets with quality values were retrieved from the Sequence Read Archive (SRA) in NCBI with the prefetch SRA-downloading tool within the SRA toolkit. The sequences associated with mussel, shrimp, and snail symbionts were excluded from further analysis. A total of 1,363 high-throughput sequence datasets were used for microbial community analyses, which mapped to V3 to V9 hypervariable regions of the full-length 16S rRNA gene sequence (see the Source Data 2). To analyze all the sequences as a pool, they were combined and clustered using a reference-based method, i.e., the Usearch v11 pipelines 67 with the Silva Release 138.2 full-length 16S rRNA gene database as reference. First, a Java tool, AlienTrimmer 68 , was used to trim primers. Subsequently, a collection of high-quality sequences was retained through the usearch fastx_filter script. The usearch closed_ref script was used to cluster sequences into taxonomies with similarity thresholds of 0.75, 0.865, and 0.945 at phylum, family, and genus levels, respectively 69 . The relative abundances of the microbial compositions were calculated based on the taxonomic information using the usearch -sintax_summary script. LEfSe (linear discriminant analysis [LDA] effect size) was performed to detect differentially abundant taxa using the “microeco” R package. A DNCI framework was used to evaluate the relative effects of general dispersal vs. niche-based processes for each group of microbial communities, which was conducted using the R package “DNCImper”. To evaluate the overall diversity, the sequences from the c sample were clustered using a non-referenced method, a Usearch pipeline at a 0.945 similarity level. 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Genomics 102:500–506 Yarza P et al (2014) Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12:635–645 Additional Declarations There is NO Competing Interest. Supplementary Files ExtendedDataFig.s20250816.pptx Extended Data Supplementarymaterial20250911.docx Supplementary Material Cite Share Download PDF Status: Posted 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. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-7588813","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":519595377,"identity":"dcb9ecb7-2f44-46ae-9177-de7b99323ef1","order_by":0,"name":"Weiguo Hou","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAA6klEQVRIiWNgGAWjYFACxgYgcYCBgb0BwSZSC88BorWAAVCZRAKRWgyONze/5qm4I2dw8/Ezya87GOT4biQwfi7Ap+XMwTZrnjPPjA1up5lJy55hMJa8kcAsPQOPFrMbiW3GvG2HEzfczmGTlmxjSNxwI4GNmQeflvsPoVpungFrqSes5QZj82Owlhs8bJIf2xgSDAhpsT+T2MY458xhY8kzacbWjGckDGeeedgsjU+LZPvxxx/eVByW4zt++OHNnzts5PmOJx/8jE8LELBJwFhA94DY4NjBC5g/wFiMPwipHQWjYBSMghEJAF5pVKDP1cKrAAAAAElFTkSuQmCC","orcid":"","institution":"China University of Geosciences, Beijing","correspondingAuthor":true,"prefix":"","firstName":"Weiguo","middleName":"","lastName":"Hou","suffix":""},{"id":519595378,"identity":"ae3ca190-6ff2-4494-846c-5fc58c1042b1","order_by":1,"name":"Shang Wang","email":"","orcid":"","institution":"Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences (CAS)","correspondingAuthor":false,"prefix":"","firstName":"Shang","middleName":"","lastName":"Wang","suffix":""},{"id":519595379,"identity":"5a8d725b-8870-45be-85a0-3156d6e2a3a8","order_by":2,"name":"Hongyu Chen","email":"","orcid":"","institution":"China University of Geosciences, Beijing","correspondingAuthor":false,"prefix":"","firstName":"Hongyu","middleName":"","lastName":"Chen","suffix":""},{"id":519595380,"identity":"d037c761-9d0d-4eb3-948b-a328bba22911","order_by":3,"name":"Hanhui Liu","email":"","orcid":"","institution":"China University of Geosciences, Beijing","correspondingAuthor":false,"prefix":"","firstName":"Hanhui","middleName":"","lastName":"Liu","suffix":""},{"id":519595381,"identity":"4e60914f-433c-4c39-92bf-b6a8aabb7f71","order_by":4,"name":"Yidi Zhang","email":"","orcid":"","institution":"China University of Geosciences, Beijing","correspondingAuthor":false,"prefix":"","firstName":"Yidi","middleName":"","lastName":"Zhang","suffix":""},{"id":519595382,"identity":"9e8695b1-5e47-459f-ab04-4264af427a16","order_by":5,"name":"Fangru Li","email":"","orcid":"","institution":"China University of Geosciences, Beijing","correspondingAuthor":false,"prefix":"","firstName":"Fangru","middleName":"","lastName":"Li","suffix":""},{"id":519595383,"identity":"1d29a08f-5ed5-49d2-8bdd-1e3b102d5c2c","order_by":6,"name":"Xiqiu Han","email":"","orcid":"https://orcid.org/0000-0001-9285-0915","institution":"Second Institute of Oceanography, Ministry of Natural Resources","correspondingAuthor":false,"prefix":"","firstName":"Xiqiu","middleName":"","lastName":"Han","suffix":""},{"id":519595384,"identity":"0865badb-7d25-443e-a121-b6ed1a70ac76","order_by":7,"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":"2025-09-11 07:20:33","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-7588813/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-7588813/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":92242394,"identity":"1e7b8772-b420-4e15-a203-387888bf20fd","added_by":"auto","created_at":"2025-09-26 08:57:16","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":455493,"visible":true,"origin":"","legend":"\u003cp\u003eEvolution of energy metabolism. The grey arrow represents the evolution timeline labeled with times in billion years ago (Ga) when the CAT lineages at the family level formed or diverged from their adjacent sister lineages. The upper major branch represents the evolution of Campylobacterota phylum, while the lower major branch represents the evolution of Thermosulfidibacterota-Aquificota phyla. The sub-branches in green, blue, and orange colours represent CAT families evolved at varying stages. Yellow bars represent the evolution of energy metabolism pathways. The divergence times were retrieved from the online TimeTree resource and references therein\u003csup\u003e44\u003c/sup\u003e.\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-7588813/v1/0c28fd7d74b9803cc5be52be.png"},{"id":92241599,"identity":"efdd0d74-8ebd-4022-a67b-7ef4470565a3","added_by":"auto","created_at":"2025-09-26 08:41:14","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":828519,"visible":true,"origin":"","legend":"\u003cp\u003eGlobal distribution of the CAT families. (a) The relative abundances of the CAT families at the phylum level; (b) the relative abundances of the anaerobic CAT families at the family level; (c) the relative abundances of the facultatively aerobic CAT families at the family level; (d) the Circos plot showing the differential distribution of the CAT families in different oceans.\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-7588813/v1/1f25dc97e6e77067506d1bef.png"},{"id":92240734,"identity":"a6ed3e2c-e3e6-4d34-bd62-e70b2bb1e2fc","added_by":"auto","created_at":"2025-09-26 08:33:14","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":302043,"visible":true,"origin":"","legend":"\u003cp\u003eComparison of the diversity of the CAT phyla from the oceans. (a-c) Comparison of the species richness (SR, the observed numbers of the OTUs) of the three phyla from the samples in the different oceans; (d-f) comparison of the phylogenetic diversity (PD) of the three phyla from the samples in the different oceans. The Red Sea was not included for its extremely low CAT diversity, and the PD values were not applicable for calculation.\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-7588813/v1/74c25c91b01ec3305777f40f.png"},{"id":92241742,"identity":"48a3b0fe-931d-4cb7-b737-4b3dbcabb41c","added_by":"auto","created_at":"2025-09-26 08:49:14","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":346694,"visible":true,"origin":"","legend":"\u003cp\u003eConceptual figure for evolution of the CAT families through Earth’s history. The seawater chemistry is based on references\u003csup\u003e20,22,23\u003c/sup\u003e, and oceanic temperature estimates follow reference\u003csup\u003e57\u003c/sup\u003e. The frame colors indicate the redox stage of seawater, ranging from reduced to oxidized conditions. Circles within the panels represent hydrothermal vents (HVs). The relative sizes of chemical species indicate their approximate concentrations\u003csup\u003e23\u003c/sup\u003e. M\u003csup\u003e2+\u003c/sup\u003e denotes divalent metal ions. Chemical species highlighted in red represent potential energy sources for the CAT families.\u003c/p\u003e","description":"","filename":"4.png","url":"https://assets-eu.researchsquare.com/files/rs-7588813/v1/6ba5bd93446e68d7efbe043b.png"},{"id":92242397,"identity":"6bbb3d49-a9c1-4a4c-a9c2-d5bbb0dbde03","added_by":"auto","created_at":"2025-09-26 08:58:03","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":2155704,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-7588813/v1/4859b260-0dbf-4218-84c2-f80fb3636eee.pdf"},{"id":92240735,"identity":"5eab887d-cf16-41aa-8fa9-ca420ec8b23b","added_by":"auto","created_at":"2025-09-26 08:33:14","extension":"pptx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":215138,"visible":true,"origin":"","legend":"Extended Data","description":"","filename":"ExtendedDataFig.s20250816.pptx","url":"https://assets-eu.researchsquare.com/files/rs-7588813/v1/a526e534f8913cec31e9b812.pptx"},{"id":92240736,"identity":"b32b95e2-883c-4724-9e46-62e6d9c0468a","added_by":"auto","created_at":"2025-09-26 08:33:14","extension":"docx","order_by":2,"title":"","display":"","copyAsset":false,"role":"supplement","size":2586632,"visible":true,"origin":"","legend":"Supplementary Material","description":"","filename":"Supplementarymaterial20250911.docx","url":"https://assets-eu.researchsquare.com/files/rs-7588813/v1/224d2ff4c25f5267f171428d.docx"}],"financialInterests":"There is \u003cb\u003eNO\u003c/b\u003e Competing Interest.","formattedTitle":"Plate Tectonic History and Ocean Oxygenation Shaping Biogeography of Hydrothermal Bacterial Community","fulltext":[{"header":"Main","content":"\u003cp\u003eThe determinants of geographic range size represent a central question in macroecology. Syntheses of studies across plants and animals confirm that dispersal ability is a foundational, albeit variable, predictor of species\u0026apos; distributions\u003csup\u003e1,2\u003c/sup\u003e. For microorganisms, however, the classic tenet that \u0026lsquo;everything is everywhere, but the environment selects\u0026rsquo; has long implied that their immense population sizes and dispersal potential negate the influence of geographic barriers\u003csup\u003e3\u003c/sup\u003e. This paradigm is increasingly challenged by evidence of endemism in isolated habitats\u003csup\u003e4,5\u003c/sup\u003e \u003csup\u003e6\u003c/sup\u003e, raising a critical question: can large-scale geological processes impose dispersal limitations sufficient to structure the global distribution of microorganisms?\u003c/p\u003e\n\u003cp\u003eHydrothermal vent systems, emerging along mid-ocean ridges and subduction-related back-arc basins, discharge reducing fluids rich in energy sources such as H₂, H₂S, CH₄, and reduced metals.These fluxes establish steep physico-chemical gradients that sustain prolific chemosynthetic ecosystems\u003csup\u003e7-9\u003c/sup\u003e. Among the key microbial colonists are members of the phyla Campylobacterota (formerly Epsilonproteobacteria), Aquificota, and Thermosulfidibacterota\u003csup\u003e10,11\u003c/sup\u003e. These taxa, collectively termed the CAT phyla, include anaerobic and microaerophilic lineages that are highly adapted to vent conditions\u003csup\u003e12-14\u003c/sup\u003e. Their ecological fidelity is profound: CAT abundances track vent activity, declining precipitously upon vent quenching\u003csup\u003e15-18\u003c/sup\u003e. Such strict habitat dependence and limited dispersal potential make the CAT phyla ideal model organisms for probing biogeographic controls in the deep sea.\u003c/p\u003e\n\u003cp\u003eThe distribution of vent habitats itself is a product of planetary-scale tectonic processes. Plate motions continuously create and destroy vent systems over millions of years\u003csup\u003e19\u003c/sup\u003e, while concurrent shifts in global ocean redox state\u003csup\u003e20\u003c/sup\u003e, especially the global oxygenation of the deep ocean\u003csup\u003e21,22\u003c/sup\u003e, fundamentally altered the biogeochemical context for anaerobic life\u003csup\u003e23\u003c/sup\u003e. Yet, the extent to which these deep-time geological events have imprinted the contemporary biogeography of vent microbiomes is entirely unknown.\u003c/p\u003e\n\u003cp\u003eHere, we synthesize global microbial community data from deep-sea vents with paleo-oceanographic reconstructions to test the hypothesis that plate tectonics has shaped modern distributions of CAT lineages. We demonstrate that their biogeography is not random but reflects the timing of ocean basin formation and oxygenation, providing evidence that geological history mediates microbial dispersal and diversification across the oceans.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eA brief review of the tectonic and geochemical evolution history of the global oceans\u003c/p\u003e\n\u003cp\u003eThe Wilson Cycle posits that periodic opening and closing of ocean basins, driven by plate tectonics\u003csup\u003e19\u003c/sup\u003e, continuously generates and eliminates hydrothermal vent habitats. The modern Pacific Ocean initiated formation at ~190 million years ago (Ma) within the vast Panthalassic Ocean (the proto-Pacific Ocean)\u003csup\u003e24\u003c/sup\u003e, which itself originated from the breakup of Rodinia during the Neo-Proterozoic (around 700-600 Ma)\u003csup\u003e25\u003c/sup\u003e. The Mediterranean Sea represents a remnant of the Paleo-Tethys Ocean, which opened during the Neoproterozoic (around 650 Ma)\u003csup\u003e26-29\u003c/sup\u003e. The Arctic Ocean is bounded by continental shelves and cratonic blocks, including the Canadian Arctic Islands, Greenland, North American, the Barents Shelf, the Baltic Shield, and Siberian\u003csup\u003e30\u003c/sup\u003e. It comprises the Amerasia and Eurasia Basins, which formed at ~ 140 Ma and ~ 56 Ma, respectively\u003csup\u003e31,32\u003c/sup\u003e. Prior to the Arctic Ocean, the extinct South Anyui Ocean existed within the circum-Arctic region, which opened around 400 Ma\u003csup\u003e31,33,34\u003c/sup\u003e. In contrast, the Atlantic and Indian Oceans are comparatively young, having formed between ~ 195 Ma and 130 Ma following the breakup of the Pangaea super-continent\u003csup\u003e35-37\u003c/sup\u003e. The Red Sea\u0026mdash;the youngest ocean hosting hydrothermal vents\u0026mdash;initiated rifting ~25-30 Ma with the separation of the Arabian-Nubian Shield\u003csup\u003e38,39\u003c/sup\u003e. We therefore hypothesize that microbial communities in hydrothermal systems of the Pacific, Mediterranean, and Arctic Oceans were inherited from pre-existing oceanic systems, whereas those in the Atlantic, Indian, and Red Sea were colonized via dispersal from adjacent oceans.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eSince the Proterozoic, ocean chemistry has undergone dramatic changes as a result of oxygenation\u003csup\u003e40\u003c/sup\u003e. Before the Proterozoic Eon (4.0-2.5 billion years ago, Ga), the global oceans were pervasively anoxic. The Proterozoic (2.5-0.54 Ga) marked the onset of surface ocean oxygenation, followed by stepwise increases throughout the Phanerozoic (540 Ma), culminating in fully oxygenated deep oceans by the early Paleozoic (~440-420 Ma)\u003csup\u003e21\u003c/sup\u003e. This trend was episodically interrupted by Mesozoic oceanic anoxic events (OAEs; 183 to 85 Ma), each lasting ~1.5 Ma \u003csup\u003e41,42\u003c/sup\u003e. These redox shifts progressively transformed seawater from a reducing chemistry rich in Fe\u003csup\u003e2+\u003c/sup\u003e, H\u003csub\u003e2\u003c/sub\u003eS, H\u003csub\u003e2\u003c/sub\u003e, S\u003csup\u003e0\u003c/sup\u003e, CH\u003csub\u003e4\u003c/sub\u003e, through a stratified state with oxic surface and anoxic deep waters, to a fully oxygenated system dominated by O\u003csub\u003e2\u003c/sub\u003e, SO\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e2-\u003c/sup\u003e, and NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e\u003csup\u003e20,21\u003c/sup\u003e. Temporally, the Pacific Ocean, Arctic Ocean, and the Mediterranean Sea originated prior to full ocean oxygenation, whereas the Atlantic, Indian oceans, and the Red Sea opened after deep ocean oxygenation. This temporal dichotomy may provide a first-order control on the assembly and evolution of vent microbial communities through geologic time.\u003c/p\u003e\n\u003cp\u003eThe evolution of the energy metabolism of the CAT phyla\u003c/p\u003e\n\u003cp\u003eWithin the CAT phyla, Campylobacterota and Aquificota contain both anaerobic and facultatively aerobic vent-specific families\u003csup\u003e43\u003c/sup\u003e. An evolutionary relationship among the families within the CAT phyla was inferred from the topography of the 120-concatenated-protein phylogeny (Fig. S1). The energy metabolism capacities were inferred from the isolate descriptions (supplementary material Table S1 and references therein) and the existence of genes responsible for metabolisms of hydrogen-, sulfur-oxidization, and sulfur-, nitrate-, and oxygen-reduction in the metagenome-assembled genomes (MAGs) (supplementary material Fig. S2-S6). The Campylobacterota phylum diverged from the Aquificota-Thermosulfidibacterota phyla at around 4.1 Ga, with a similar evolutionary history of energy metabolisms (Fig. 1). From the early-diverged families to the late-diverged lineages, the energy metabolism pathways become increasingly complex. The earliest evolved families (i.e., Thermosulfidibacteraceae, Desulfurobacteriaceae, and Hippeaceae, formed at 2.08-2.85 Ga) only harnessed the elemental sulfur-reduction with hydrogen for chemoautolithotrophic energy metabolism, which is also inherited by the rest of the CAT families. Then, nitrate was used as an additional electron acceptor in the families of Nautiliaceae and Desulfurobacteriaceae (formed at around 1.6 Ga), with NH\u003csub\u003e3\u003c/sub\u003e as the reducing product. At around 1.0 Ga, aerobic families (including Nitratiruptoraceae, Hydrogenimonadaceae, Sulfurovaceae, Sulfurimonadaceae, Hydrogenothermaceae, and Aquificaceae) formed, accompanied by an increase of sulfur species as electron donors, such as sulfide and thiosulfate, and molecular O\u003csub\u003e2\u003c/sub\u003e as the electron acceptor. Synchronously, the reducing products of nitrate shifted from NH\u003csub\u003e3\u003c/sub\u003e to N\u003csub\u003e2\u003c/sub\u003e or N\u003csub\u003e2\u003c/sub\u003eO (Fig. 1).\u003c/p\u003e\n\u003cp\u003eGlobal distribution pattern of the CAT families\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eMicrobial community compositions, based on 16S rRNA gene amplicon data at the family level, revealed a pronounced divergence in the abundance of CAT families between ancient and younger oceans. Linear discriminant analysis (LDA) confirmed that the relative abundances of CAT families were significantly higher in early-formed oceans (Pacific and Arctic Oceans, and Mediterranean Sea) compared to the late-formed systems (Atlantic and Indian Oceans, and Red Sea) (Supplementary material Figures S7-S16). This disparity was visually evident in abundance-projected global maps\u0026nbsp;(Fig. 2), which showed Campylobacterota were ubiquitous and highly abundant (\u0026gt;50% relative abundance) across most sampling sites, except in the Indian Ocean, South Atlantic Ocean, and Red Sea (Fig. 2a). Aquificota were prevalent (\u0026gt; 10% relative abundance) in the Pacific and Arctic Oceans, and Mediterranean Sea, while Thermosulfidibacterota occurred at lower abundances (\u0026gt; 1%), peaking in the Arctic Ocean near 10%.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eObligately anaerobic lineages (Thermosulfidibacterota, Desulfurobacteriaceae, Nautiliaceae, Hippeaceae, and Desulfurellaceae) exhibited highly restricted distributions, with Desulfurobacteriaceae concentrated in the eastern Pacific, Hippeaceae and Desulfurellaceae largely confined to the Gulf of California (Fig. 2b). Notably, no anaerobic CAT members were detected in the Indian or South Atlantic Oceans. In contrast, facultatively aerobic families (Sulfurovaceae, Sulfurimonadaceae, Nitratiruptoraceae, Aquificae, and Hydrogenothermaceae) showed broader distributions (Fig. 2c), consistent with their respective phyla (Fig. 2a). Among them, Sulfurimonadaceae and Sulfurovaceae were the most abundant CAT families globally (Fig. 2d).\u003c/p\u003e\n\u003cp\u003eAlpha diversity analyses further revealed systematic differences in the richness and phylogenetic diversity of CAT taxa across oceans. Hydrothermal vent systems in the Pacific Ocean exhibited the highest species richness (SR) and phylogenetic diversity (PD) for all three CAT phyla (Fig. 3). Campylobacterota (Fig. 3a\u0026amp;d) and Aquificota (Fig. 3b\u0026amp;e) showed significantly greater SR and PD in the Pacific compared to all other regions. Thermosulfidibacterota diversity was also highest in the Pacific, comparable to the Arctic Ocean (Fig. 3c\u0026amp;g). In contrast, the late-formed oceans\u0026mdash;the Atlantic, Indian, and Red Sea\u0026mdash;consistently hosted relatively lower CAT diversity (Fig. 3). Across all regions, taxonomic richness declined in the order: Campylobacterota \u0026gt; Aquificota \u0026gt; Thermosulfidibacterota. Together, these results demonstrate a clear biogeographic imprint of ocean basin ages on the diversity and distribution of hydrothermal vent microbiomes.\u003c/p\u003e\n\u003cp\u003eThe mechanism of the uneven distribution of the CAT families in the oceans\u003c/p\u003e\n\u003cp\u003eThe assembly of microbial communities is governed by both deterministic (niche-based) and stochastic (dispersal-driven) processes\u003csup\u003e45,46\u003c/sup\u003e. To quantify their relative contributions to the biogeographic patterns of CAT families, we applied the dispersal\u0026ndash;niche continuum index (DNCI)\u003csup\u003e47,48\u003c/sup\u003e, a metric derived from a permutation-based framework (PER-SIMPER) that uses taxon occurrence data to disentangle assembly mechanisms\u003csup\u003e48,49\u003c/sup\u003e. Consistently negative DNCI values indicated that dispersal limitation, rather than niche selection, was the dominant driver of community dissimilarity between the early-formed (Pacific, Arctic, and Mediterranean) and the late-formed (Atlantic, Indian, and Red Sea) oceans (Table 1, Supplementary material Fig. S17). This pattern held for pairwise comparisons between adjacent oceans (Table 1, Supplementary material Fig. S18-S26). LefSe analysis further identified both anaerobic and facultatively aerobic CAT families as key biomarkers differentiating vent communities worldwide (Table 1, Supplementary material Fig. S7-S16), supporting the inference that their limited dispersal capacity underlies large-scale biogeographic divergence.\u003c/p\u003e\n\u003cp\u003eTable 1 DNCI values between pairwise groups of hydrothermal microbial communities\u0026nbsp;\u003c/p\u003e\n\u003ctable border=\"1\" cellspacing=\"0\" cellpadding=\"0\"\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eOceanic pair groups\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eDNCI values\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eS.DNCI\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eCAT families with differential distribution\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eEarly-Late\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e-9.865961\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e0.06405824\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eAquificaceae, Sulfurovaceae, Sulfurimonadaceae, Nautiliaceae, Hydrogenothermaceae, Desulfurobacteriaceae, B14-G1, Hydrogenimonadaceae, Hippeaceae, Desulfurellaceae, Thermosulfidibacteraceae, and Nitratiruptoraceae\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003ePacific-Arctic\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e-8.6011656\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e0.11960298\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eSulfurimonadaceae, Sulfurovaceae, Nautiliaceae, and Hydrogenothermaceae\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003ePacific-Atlantic\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e-52.6056211\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e0.08219519\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eThermosulfidibacteraceae, Hydrogenothermaceae, Desulfurobacteriaceae, Aquificaceae, Desulfurellaceae, Nitratiruptoraceae, Hippeaceae, and B14-G1\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003ePacific-Indian\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e-17.9522868\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e0.12904323\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eSulfurimonadaceae, Nautiliaceae, Thermosulfidibacteraceae, Desulfurobacteriaceae, Nitratiruptoraceae, and Hippeaceae\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003ePacific-Mediterranean\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e-219.8926051\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e0.26002027\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eSulfurovaceae, Sulfurimonadaceae, Nautiliaceae, Thermosulfidibacteraceae, Aquificaceae, Desulfurellaceae, Desulfurobacteriaceae, and Hippeaceae\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eMediterranean_Atlantic\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e-40.1411662\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e0.07002511\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eHydrogenothermaceae, Nitratiruptoraceae, Sulfurimonadaceae, and B14-G1; Nautiliaceae\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eMediterranean-Indian\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e-100.2812506\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e0.77249686\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eNitratiruptoraceae; Hydrogenimonadaceae and Nautiliaceae\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eArctic-Atlantic\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e-9.7230757\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e0.31240003\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eDesulfurobacteraceae, Thermosulfidibacteraceae, and B14-G1\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eIndian-Atlantic\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e-29.3061837\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e0.26081572\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eHydrogenimonadaceae\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eIndian-Red Sea\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e-59.2821389\u0026nbsp;\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003e0.52192536\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd valign=\"top\"\u003e\n \u003cp\u003eSufurovaceae, Sulfurimonadaceae, Hydrogenothermaceae, and Aquificaceae\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n\u003c/table\u003e\n\u003cp\u003eThe deep ocean is thought to have become fully oxygenated by the late Paleozoic (~420 Ma)\u003csup\u003e50,51\u003c/sup\u003e. Molecular oxygen is toxic to anaerobic microorganisms, damaging biomolecules via reactive oxygen species and oxidizing low-redox-potential metalloenzymes\u003csup\u003e52\u003c/sup\u003e. Consistent with this, anaerobic CAT lineages encode significantly fewer antioxidant enzymes in their MAGs than aerobic counterparts (Extended Data Fig. 1), indicating poor oxygen tolerance and constrained dispersal through oxic waters. This explains the near-absence of anaerobic CAT families in the younger Indian Ocean and Red Sea (Fig. 3c). Most anaerobic lineages are instead confined to the Pacific, Arctic, and Mediterranean Oceans (Fig. 2b), consistent with their origins predating deep-sea oxygenation\u003csup\u003e50,51\u003c/sup\u003e (Fig. 1).\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eTheoretically, the fully oxygenated Atlantic should also exclude anaerobic taxa, yet we detected Nautiliaceae in the North Atlantic (Fig. 3c). We propose that Mesozoic oceanic anoxic events (OAEs) may have facilitated their dispersal into the Central Atlantic Ocean (Fig. 2b), which opened earlier than other parts of the Atlantic Ocean and remained connected to the Pacific Ocean\u003csup\u003e33,37\u003c/sup\u003e.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eOxygenation also diminishes the availability of reduced compounds (e.g., H\u003csub\u003e2\u003c/sub\u003e, H\u003csub\u003e2\u003c/sub\u003eS, S\u003csup\u003e0\u003c/sup\u003e, SO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e2-\u003c/sup\u003e, S\u003csub\u003e2\u003c/sub\u003eO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e2-\u003c/sup\u003e) that serve as energy sources for facultatively aerobic CAT families, likely limiting their dispersal even in the presence of oxygen. Indeed, low abundances of the facultatively aerobic Hydrogenothermaceae, Sulfurovaceae, and Sulfurimonadaceae were observed in the Central and Southwest Indian Ocean (Fig. 2c), and Nitratiruptoraceae was sparse in the Northwest Indian Ocean, South Atlantic Ocean, and Red Sea. Further support comes from the Loihi hydrothermal field (~400 ka) in the Pacific, where newly formed vents host low abundances of facultative aerobic CAT families\u003csup\u003e53\u003c/sup\u003e, highlighting their slow colonization under modern oxidizing conditions. Nevertheless, specific lineages such as Sulfurimonadaceae (mainly genus \u003cem\u003eSulfurimonas\u003c/em\u003e) and Sulfurovaceae (mainly genus \u003cem\u003eSulfurovum\u003c/em\u003e) can disperse via particle-rich hydrothermal plumes that contain micro-niches with reduced compounds, providing a mechanism for long-range dispersal in oxic waters\u003csup\u003e54-56\u003c/sup\u003e.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eDistribution of CAT taxa through Earth\u0026rsquo;s redox history\u003c/p\u003e\n\u003cp\u003eThe evolution trajectory of CAT lineages reflects major transitions in ocean redox chemistry, which can be divided into anoxic, intermediate, and oxic stages\u003csup\u003e20\u003c/sup\u003e. During the anoxic stage (prior to ~ 2.45 Ga), the global ocean was rich in reduced compounds such as Fe\u003csup\u003e2+\u003c/sup\u003e, H\u003csub\u003e2\u003c/sub\u003e, S\u003csup\u003e0\u003c/sup\u003e, H\u003csub\u003e2\u003c/sub\u003eS, and NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e (Fig. 4a)\u003csup\u003e22,23\u003c/sup\u003e, resembling the chemical environment of contemporary hydrothermal vent fluids. High ocean temperatures (~65 - 80 \u003csup\u003eo\u003c/sup\u003eC) \u003csup\u003e57\u003c/sup\u003e were near the optimal growth temperature (OGT) for the early-evolved CAT lineages (Extended Data Fig. 2), implying that ancestral CAT taxa (such as Thermosulfidibacterota, Hippeaceae, and Desulfurellaceae) were likely ubiquitous in the open ocean rather than vent-restricted.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eThe Great Oxygenation Event (GOE) marked the onset of an intermediate phase, oxidizing surface waters and driving the accumulation of NO\u003csub\u003e2\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e, NO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e-\u003c/sup\u003e, and SO\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e2-\u003c/sup\u003e from reduced precursors (e.g., NH\u003csub\u003e4\u003c/sub\u003e\u003csup\u003e+\u003c/sup\u003e, S\u003csup\u003e0\u003c/sup\u003e, and H\u003csub\u003e2\u003c/sub\u003eS), while simultaneously decreasing H\u003csub\u003e2\u003c/sub\u003e availability in the deep ocean (Fig. 4b)\u003csup\u003e22,23\u003c/sup\u003e. Episodic deep-ocean oxygenation\u003csup\u003e58,59\u003c/sup\u003e likely promoted metabolic diversification within CAT lineages, favoring taxa capable of utilizing a wider array of electron acceptors. Lineages relying exclusively on H₂ as a sole electron donor (e.g., Desulfurobacteriaceae, Hautiliaceae, and Hydrogenimonadaceae) became increasingly restricted to hydrothermal vents, where H₂ remained abundant. In contrast, sulfur-oxidizing CAT families continued to proliferate in broader marine settings due to the persistence of S⁰, H\u003csub\u003e2\u003c/sub\u003eS, and S\u003csub\u003e2\u003c/sub\u003eO\u003csub\u003e3\u003c/sub\u003e\u003csup\u003e2\u003c/sup\u003e⁻ in seawater.\u003c/p\u003e\n\u003cp\u003eBy the Phanerozoic (~0.54 Ga onward), full ocean oxygenation\u003csup\u003e40\u003c/sup\u003e dramatically reduced the pool of reduced chemicals in the open ocean (Fig. 4c). As a result, both anaerobic and facultatively aerobic CAT taxa became largely confined to hydrothermal vent systems, where reductants remained plentiful. The sharp redox gradients between oxidized seawater and reduced vent fluids sustained high energy availability, fueling diverse microbial ecosystems at modern vents. Thus, the progressive oxygenation of Earth\u0026rsquo;s oceans systematically narrowed the ecological niches of CAT lineages, transforming them from widespread marine taxa into specialists of hydrothermal systems.\u0026nbsp;\u003c/p\u003e"},{"header":"Summary","content":"\u003cp\u003eWe reveal a pronounced biogeographic disjunction between ancient oceans formed under anoxic conditions (Pacific, Arctic, Mediterranean) and younger, oxygen-rich basins (Atlantic and Indian). In this study, we demonstrate that the biogeography of hydrothermal vent-specific bacteria, notably the CAT phyla (Campylobacterota, Aquificota, and Thermsulfidibacterota), is fundamentally shaped by the tectonic and geochemical evolution of oceans. We show that early-formed oceans (Pacific, Arctic, and Mediterranean Oceans) host significantly higher diversity and abundance of CAT lineages, including numerous anaerobic groups. In contrast, late-formed oceans (Atlantic, Indian Oceans, and the Red Sea) contained fewer CAT taxa, predominantly comprising aerobic families. This distribution reflects the interplay between ocean formation age and Earth’s redox history. Specifically, the Pacific, Arctic, and Mediterranean Oceans originated during periods of widespread anoxia, facilitating the unrestricted dispersal and establishment of anaerobic vent microbes. Conversely, the Atlantic and Indian Oceans formed after deep-ocean oxygenation, which imposed a dual constraint: molecular oxygen limited the dispersal of anaerobic taxa, while the diminished availability of reduced chemical compounds reduced energy supplies even for aerobic vent specialists. Our findings directly link plate tectonic processes and planetary-scale geochemical transitions to the assembly and distribution of microbial life. By revealing how deep-time geological events structured contemporary microbial biogeography, this study establishes a new framework for understanding the origins and dispersal of life in Earth’s subsurface biosphere.\u003c/p\u003e"},{"header":"Methods","content":"\u003cp\u003eA total of 1,192 Metagenome-assembled genomes (MAGs) affiliated with the phyla Campylobacterota, Aquificota, and Thermosulfidibacterota were retrieved from the NCBI database with the “Download Genome Taxon” function in the dataset tool. The taxonomy of the MAGs was verified using the GTDB-tk v0.3.3 tool\u003csup\u003e\u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e60\u003c/span\u003e\u003c/sup\u003e. Non-hydrothermal vent-derived MAGs were excluded from further analysis. The qualities of all retrieved MAGs were evaluated with CheckM v1.2.2. Any MAGs with completeness \u0026gt; 0.5 and contamination \u0026lt; 0.1 were selected for subsequent analyses. After quality filtering, 923 MAGs were targeted for further analysis (see the Source Data 1). The optimal growth temperatures (OGTs) of the MAGs were predicted using the TOME software\u003csup\u003e\u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e61\u003c/span\u003e\u003c/sup\u003e. The phylogenetic relationship of the CAT families was inferred from the concatenated 120 marker genes of the MAGs, which were identified, concatenated, and aligned using the GTDB-tk v0.3.3 tool\u003csup\u003e\u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e60\u003c/span\u003e\u003c/sup\u003e. A Maximum Likelihood tree was constructed using MEGA-12 software with the Jones-Taylor-Thornton model substitution with a bootstrap value of 1000\u003csup\u003e62\u003c/sup\u003e.\u003c/p\u003e\u003cp\u003eOpen reading frames (ORFs) of the MAGs were predicted with Prodigal v2.6.3. The predicted ORFs were searched against the NCBI nr protein database (2019/07) and eggNOG database with the BLASTP algorithm (coverage of \u0026gt; 75%, e-values of \u0026lt; 1 × 10\u003csup\u003e− 20\u003c/sup\u003e) to check their protein identities to the most closely related sequences using DIAMOND sequence aligner version 0.9.30.131 (\u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttp://github.com/bbuchfink/diamond\u003c/span\u003e\u003cspan address=\"http://github.com/bbuchfink/diamond\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e). Then, the genes related to energy metabolism pathways, including nitrogen cycling\u003csup\u003e\u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e63\u003c/span\u003e\u003c/sup\u003e, sulfur cycling\u003csup\u003e\u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e64\u003c/span\u003e\u003c/sup\u003e, oxygen reductases\u003csup\u003e\u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e65\u003c/span\u003e\u003c/sup\u003e, and hydrogenases\u003csup\u003e\u003cspan citationid=\"CR66\" class=\"CitationRef\"\u003e66\u003c/span\u003e\u003c/sup\u003e, as well as the antioxidases in each MAG, were counted using a Linux searching tool \u003cem\u003egrep\u003c/em\u003e. The types of oxygen-respiration enzymes and hydrogenases were also analyzed using DIAMOND by searching against the Heme-Copper Oxidases (HCOs) and Hydrogenase databases\u003csup\u003e\u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e65\u003c/span\u003e,\u003cspan citationid=\"CR66\" class=\"CitationRef\"\u003e66\u003c/span\u003e\u003c/sup\u003e. These targeted genes were also verified using the online Conserved Domain Search Service (CD Search) in the NCBI web (\u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi\u003c/span\u003e\u003cspan address=\"https://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e).\u003c/p\u003e\u003cp\u003eThe hydrothermal vent-related high-throughput 16S rRNA gene sequence datasets with quality values were retrieved from the Sequence Read Archive (SRA) in NCBI with the \u003cem\u003eprefetch\u003c/em\u003e SRA-downloading tool within the SRA toolkit. The sequences associated with mussel, shrimp, and snail symbionts were excluded from further analysis. A total of 1,363 high-throughput sequence datasets were used for microbial community analyses, which mapped to V3 to V9 hypervariable regions of the full-length 16S rRNA gene sequence (see the Source Data 2). To analyze all the sequences as a pool, they were combined and clustered using a reference-based method, i.e., the Usearch v11 pipelines\u003csup\u003e\u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e67\u003c/span\u003e\u003c/sup\u003e with the Silva Release 138.2 full-length 16S rRNA gene database as reference. First, a Java tool, AlienTrimmer\u003csup\u003e\u003cspan citationid=\"CR68\" class=\"CitationRef\"\u003e68\u003c/span\u003e\u003c/sup\u003e, was used to trim primers. Subsequently, a collection of high-quality sequences was retained through the \u003cem\u003eusearch fastx_filter\u003c/em\u003e script. The \u003cem\u003eusearch closed_ref\u003c/em\u003e script was used to cluster sequences into taxonomies with similarity thresholds of 0.75, 0.865, and 0.945 at phylum, family, and genus levels, respectively\u003csup\u003e\u003cspan citationid=\"CR69\" class=\"CitationRef\"\u003e69\u003c/span\u003e\u003c/sup\u003e. The relative abundances of the microbial compositions were calculated based on the taxonomic information using the \u003cem\u003eusearch -sintax_summary\u003c/em\u003e script. LEfSe (linear discriminant analysis [LDA] effect size) was performed to detect differentially abundant taxa using the “microeco” R package. A DNCI framework was used to evaluate the relative effects of general dispersal vs. niche-based processes for each group of microbial communities, which was conducted using the R package “DNCImper”.\u003c/p\u003e\u003cp\u003eTo evaluate the overall diversity, the sequences from the c sample were clustered using a non-referenced method, a Usearch pipeline at a 0.945 similarity level. Alpha diversity indices, including species richness (SR) and phylogenetic diversity (PD), were calculated with the Vegan R script and plotted with the Picante R script. The different significances of the diversity indices between the two groups of the microbial community were tested with a T-test using the “ggplubr” package in R. The differences were considered statistically significant when p \u0026lt; 0.05.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eAlzate A, Onstein RE (2022) Understanding the relationship between dispersal and range size. Ecol Lett 25:2303\u0026ndash;2323\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eSheth SN, Morueta-Holme N, Angert AL (2020) Determinants of geographic range size in plants. New Phytol 226:650\u0026ndash;665\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eFinlay BJ (2002) Global Dispersal of Free-Living Microbial Eukaryote Species. Science 296:1061\u0026ndash;1063\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eWhitaker RJ, Grogan DW, Taylor JW (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301:976\u0026ndash;978\u003c/span\u003e\u003c/li\u003e\u003cli\u003e\u003cspan\u003eHou W et al (2013) A comprehensive census of microbial diversity in hot springs of Tengchong, Yunnan Province China using 16S rRNA gene pyrosequencing. 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Nat Rev Microbiol 12:635\u0026ndash;645\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":true,"hideJournal":true,"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":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"hydrothermal vents, microbial community, global distribution, tectonic history, ocean oxygenation","lastPublishedDoi":"10.21203/rs.3.rs-7588813/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-7588813/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003ePlate tectonics has fundamentally shaped the biogeography and evolution of macroscopic life, but its influence on microbial distributions remains poorly understood. Here, we demonstrate that the global biogeography of hydrothermal vent-endemic microbiota —specifically, lithoautotrophic bacterial families within the phyla Campylobacterota, Aquificota, and Thermosulfidibacterota (collectively CAT families) — is structured by tectonic history. CAT families, particularly obligate anaerobes, are significantly more abundant in early-origin Pacific, Arctic, and Mediterranean oceans, whereas they are notably scarce in late-formed Atlantic and Indian Oceans. We attribute this pattern to the timing of ocean formation and its interplay with global redox evolution. During the genesis of the former three oceans, anoxic conditions facilitated the unrestricted dispersal among oceans and colonization of anaerobic CAT families in hydrothermal vents. In contrast, fully oxygenated conditions during the formation of the two later oceans imposed a dual barrier: molecular oxygen was toxic to obligate anaerobes, and the oxidation of reduced chemicals depleted the energy sources necessary for facultative aerobes. Our findings established that plate tectonics has imposed first-order constraints on microbial biogeography through long-term modulation of ocean chemistry and habitat connectivity. These results integrate microbial dispersal into a geodynamic framework, revealing that even microbial life is subject to planetary-scale geological constraints.\u003c/p\u003e","manuscriptTitle":"Plate Tectonic History and Ocean Oxygenation Shaping Biogeography of Hydrothermal Bacterial Community","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2025-09-26 08:33:10","doi":"10.21203/rs.3.rs-7588813/v1","editorialEvents":[],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"nature-communications","isNatureJournal":true,"hasQc":false,"allowDirectSubmit":false,"externalIdentity":"NCOMMS","sideBox":"Learn more about [Nature Communications](http://www.nature.com/ncomms/)","snPcode":"","submissionUrl":"https://mts-ncomms.nature.com/","title":"Nature Communications","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"ejp","reportingPortfolio":"Nature Communications","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"90e7a57f-6153-49b0-9b86-208261f8b1f0","owner":[],"postedDate":"September 26th, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[{"id":55224150,"name":"Earth and environmental sciences/Planetary science/Tectonics"},{"id":55224151,"name":"Earth and environmental sciences/Ecology/Biodiversity"},{"id":55224152,"name":"Earth and environmental sciences/Ocean sciences/Marine biology"}],"tags":[],"updatedAt":"2026-04-07T15:16:36+00:00","versionOfRecord":[],"versionCreatedAt":"2025-09-26 08:33:10","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-7588813","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-7588813","identity":"rs-7588813","version":["v1"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}