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Large-scale and multi-sample datasets have revealed that microbial diversity and geographic distribution patterns are distinct across various habitats, particularly between hydrothermal vent and cold seep ecosystems. To date, our understanding of the effects of spatial and geochemical gradients on marine microbial communities remains limited. Here, we report the microbial diversity and metabolic versatility of a remote seafloor sediment ecosystem at different sites (GC-2, -4, -5, -6, -8) in the Mid-Okinawa Trough (Mid-OT) using high-throughput metagenomic sequencing technology. Desulfobacteraceae (3.1%) were detected in a high abundance at GC-2 with intense methane concentrations (353 μL/L), which showed a clear correlation with cold seeping. Whereas Candidatus Brocadiaceae (1.7%), Rhodobacteraceae (0.9%), and Rhodospirillaceae (0.7%), which are commonly involved in denitrification and sulfur oxidation, were enriched at GC-8. Concurrently investigating the potential of deep-sea microbial metabolism, we gained insights into the adaptive capabilities and metabolic mechanisms of microorganisms within seafloor environments. Utilizing the Kyoto Encyclopedia of Genes and Genomes (KEGG) database, the analysis of functional modules revealed a significant enrichment (71–74%) of genes associated with metabolic pathways. These results expand our knowledge of the relationship between microbial biodiversity and metabolic versatility in deep-sea extreme environments. [ABSTRACT FROM AUTHOR]

The snail Provanna glabra is a dominant species inhabiting both hydrothermal vents and cold seeps of the Northwest Pacific Ocean. The genetic diversity and population structure of the snail from the hydrothermal vents of Okinawa Trough and a methane seep in the South China Sea were investigated using mitochondrial cytochrome c oxidase subunit I (COI) and genome‐wide single nucleotide polymorphisms (SNPs). A total of 28,805 SNPs were screened based on 2b‐RAD sequencing. Substantial genetic differences between vent and seep populations were identified based on the two datasets with FST = 0.753 (COI) and FST = 0.109 (SNPs), respectively. The results of phylogenetic tree, ADMIXTURE and principal component analysis jointly supported the population differentiation. Outlier detection confirmed the local adaptation of P. glabras populations, and the annotation of these outliers revealed that they were closely associated with processes of signal transduction, immunity, DNA repair, transposable elements and biological development. The genetic divergence observed between hydrothermal vent and methane seep P. glabra populations might be induced by the geographic barrier, limited dispersal ability and natural selection imposed by local environmental pressures from different deep‐sea habitats, e.g. chemical composition, temperature and microbes. These results provide a genetic basis for the microevolution of snails inhabiting deep‐sea chemosynthetic ecosystems. [ABSTRACT FROM AUTHOR]

Information on genetic divergence and migration patterns of vent‐ and seep‐endemic macrobenthos can help delimit biogeographical provinces and provide scientific guidelines for deep‐sea conservation under the growing threats of anthropogenic disturbances. Nevertheless, related studies are still scarce, impeding the informed conservation of these hotspots of deep‐sea biodiversity. To bridge this knowledge gap, we conducted a population connectivity study on the galatheoid squat lobster Shinkaia crosnieri – a deep‐sea foundation species widely distributed in vent and seep ecosystems in the Northwest Pacific. With the application of an interdisciplinary methodology involving population genomics and oceanographic approaches, we unveiled two semi‐isolated lineages of S. crosnieri with limited and asymmetrical gene flow potentially shaped by the geographic settings, habitat types, and ocean currents – one comprising vent populations in the Okinawa Trough, with those inhabiting the southern trough area likely serving as the source; the other being the Jiaolong (JR) seep population in the South China Sea. The latter might have recently experienced a pronounced demographic contraction and exhibited genetic introgression from the Okinawa Trough lineage, potentially mediated by the intrusion of the North Pacific Intermediate Water. We then compared the biogeographic patterns between S. crosnieri and two other representative and co‐occurring vent‐ and seep‐endemic species using published data. Based on their biogeographical subdivisions and source‐sink dynamics, we highlighted the southern Okinawa Trough vents and the JR seep warrant imperative conservation efforts to sustain the deep‐sea biodiversity in the Northwest Pacific. [ABSTRACT FROM AUTHOR]

Iron (Fe), sulfur (S), and molybdenum (Mo) geochemistry in marine sediments impacted by hydrothermal plumes and/or cold seeps is complex and has not been systematically documented. Here we characterize Fe, S, and Mo diagenesis in sediments between the Minami‐Ensei Knoll hydrothermal field and a cold‐seep site of the middle Okinawa Trough. Results show that distances away from the hydrothermal field and the steep trough slope may significantly affect the transport of hydrothermal Fe. The transformation of hydrothermal reactive Fe to poorly reactive or unreactive Fe‐bearing phyllosilicates decreased the relative fractions of highly reactive Fe (FeHR) in total Fe (FeHR/FeT). Despite this, the standing stocks of Fe oxides in the methane‐free sediments have not been dampened, indicating no net impacts of hydrothermal Fe inputs on the size of Fe oxides. In the methane‐free sediments, low ratios of total reduced inorganic sulfide (TRIS) to total organic carbon (TOC) (TRIS/TOC), highly 34S‐depleted pyrite, and low Mo contents suggest that organoclastic sulfate reduction is at low rates and plays a limited role in carbon cycle. In the cold‐seep sediments, however, intense sulfate reduction coupled to anaerobic methane oxidation significantly elevate TRIS/TOC ratios, Mo enrichment, and isotope compositions of Mo and pyrite‐S. This pathway is expected to be important in carbon cycle in the basin due to the wide occurrence of cold seeps. Our results highlight the important controls of the local extreme depositional/diagenetic conditions on sedimentary S and Mo records, with implications for the reconstruction of paleoredox states of the past earth's surface. Plain Language Summary: Submarine methane‐rich cold seeps and hydrothermal venting exert important influences on the geochemistry of iron, sulfur, and molybdenum. However, the influences of the two extreme environments on the three interlinked elements in seafloor have not been well documented. Here, we used solid‐phase chemistry of four sediment cores located between a hydrothermal field and a cold‐seep site in the middle Okinawa Trough to document the impacts of the two extreme environments on the geochemistry of iron, sulfur, and molybdenum. Results show that hydrothermal Fe signature in the sediments is largely controlled by the distances away from the hydrothermal field and the steep slope of the trough; the hydrothermal Fe inputs have no net impacts on sedimentary iron oxide contents due to simultaneous inactivation of reactive Fe. In the methane‐free sediments, sulfate reduction (SR) is coupled mainly to oxidation of sedimentary organic carbon. In the cold‐seep site, however, SR coupled to anaerobic methane oxidation is the main pathway of carbon cycle, leading to significant enrichments of molybdenum and isotopically heavy pyrite. The differences highlight the important control of local extreme depositional/diagenetic conditions on geochemical records of iron, sulfur, and molybdenum, with implications for the reconstruction of paleoredox states in the past. Key Points: Distances away from the vent, steep basin slope and Fe inactivation control the signature of hydrothermal Fe in the basin sedimentsLow lability of organics limits sulfate reduction (SR) in CH4‐free sediments, while CH4 largely facilitates SR in cold‐seep sedimentsLocal extreme conditions exert key controls on S‐Fe‐Mo diagenesis in the basin [ABSTRACT FROM AUTHOR]

Submarine methane seepages constitute an important part of global carbon cycle and may be promoted by the dissociation of gas hydrate. The migration pattern of a seepage is commonly dominated by vertical transport of methane-rich pore fluids, and then lateral migration of these fluids probably occurred due to self-sealing effect of carbonate crust above vertical migration conduit. Some studies found the evidence of this lateral migration, but the one from the record of seep carbonate in nature is very rare. In this study, we present the results of mineralogical, isotopic, and dating analyses of a core containing seep carbonates obtained from seafloor drilling site D5 in the Middle Okinawa Trough. The core contains 0.98-m-long carbonate interval that predominantly consists of aragonite, with an average content of ∼86.6%. The carbonate exhibits moderate depletion in 13C (δ13C values: −37.2‰ to −16.3‰ Vienna Pee Dee Belemnite; VPDB) and enrichment in 18O (δ18O values: 4.3‰–5.8‰ VPDB), with relatively constant 87Sr/86Sr values (0.709167–0.709197). These results suggest that the precipitation of the seep carbonate was induced by the sulfate-driven anaerobic oxidation of methane close to the seabed and this methane could be from the dissociation of gas hydrates. U–Th age–depth profile shows that two carbonate intervals grew downwards coevally to coalesce into a thicker crust, and its upper segment also grew upwards. We interpret that lateral migration of the fluid flows at two levels are responsible for the formation of upper and lower segments of carbonate intervals because they have (a) the distinct clustering of δ13C and δ18O values and (b) a coeval period of fast growth. It is likely that upward migration of methane was redirected by self-sealing of overlying carbonate crust, leading to lateral migration at the flank of seabed mound Db4 during 6.2–4.6 ka. Our findings highlight the interaction between fluid flows and authigenic carbonates during Late Quaternary, which implies that more methane could be consumed by oxidation because it takes longer time for methane to bypass self-sealing of carbonate to escape into the ocean. • U–Th dating of aragonite-rich carbonate from a drilling core D5 in the Okinawa Trough yields ages of 6.2–4.6 ka. • Enrichment of 18O in carbonate crust indicates the contribution of gas hydrate dissociation to intensified methane seepage. • U–Th ages with depth imply the occurrences of lateral migration of methane at two depths at flank of seabed mound. • Prolonged migration due to bypassing carbonate sealing may cause more of methane consumed close to seabed at seeps. [ABSTRACT FROM AUTHOR]

Geochemistry of iron and trace metals in seep carbonates and its dependence on anaerobic oxidation of methane (AOM)-driven diagenesis in cold seeps are not well documented. Here we characterize geochemistry of Fe and trace metals in carbonate nodules collected at an active cold seep in the middle Okinawa Trough (OT) impacted by hydrothermal plumes. The carbonate nodules in the studied core are dominated by aragonite even at sulfate-low core bottom. Most aragonite at the core bottom may have formed much earlier close to the seafloor under high sulfate concentration. Additionally, porewater at the depth may not be developed to a condition for the formation of calcite dominating over aragonite due to constant downward replenishment of sulfate across through shallow SMTZ (40 cm below sediment surface). As indicated by δ13C and δ18O of the carbonates, anaerobic oxidation of thermogenic methane from gas hydrate dissociation is the dominant fluid source for carbonate precipitation. It can be inferred from the existence of vivianite that Fe reduction coupled to AOM (Fe-AOM) may have ever been prevalent at the hydrothermal Fe-impacted seep site. Enhanced inputs of Mo, Co, Cu, Ni, and Zn associated with hydrothermal Fe-oxyhydroxides-organic colloids is the main source for their high enrichment in the carbonate nodules, and clay minerals and AOM-related microbial organics may have played an important role in their partitioning in the nodules. Uranium enrichment in the carbonate nodules is mainly through enhanced U delivery associated with Fe-oxyhydroxides-scavenged organic colloids and additional U enrichment induced by U(VI) reduction. U(IV) incorporation into carbonate lattices dominates U partitioning in the carbonate nodules over the upper 60 cm of the seep sediments, but the incorporation is substantially dampened at depth due to an increase in concentration of dissolved inorganic carbon, which consequently may have rendered U(IV) adsorption on clay minerals as the important U sink in the nodules. Our results suggest that the exceptional enrichments of Co, Cu, Ni, Zn, Mo, and U in seep carbonates may be used as a paleo-proxy to differentiate cold-seep carbonates whose formation has been co-impacted by hydrothermal plumes. • Aragonite is the dominant carbonate mineral even at sulfate-poor core bottom. • Carbonate formation is related to AOM and hydrate dissociation. • Hydrothermal Fe input enhances trace metal enrichment in carbonate nodules. • Clays and AOM-microbial organics play an important role in trace metal partitioning. [ABSTRACT FROM AUTHOR]

[Display omitted] • Carbonates in sediments of the Okinawa Trough are biogenic and authigenic in origin. • Authigenic carbonate in sediments of the Okinawa Trough is mainly high-Mg calcite. • The negative carbon isotope values reflect the origin of authigenic carbonate from AOM. • Biogenic carbonate contents were low (high) during the glacial (interglacial) period. The elemental and isotopic compositions and abundance of carbonates in marine sediments are used to reconstruct ancient climate and ocean conditions. These carbonates usually include biogenic and authigenic carbonates in origin, which are controlled by sedimentary and diagenetic processes, respectively. However, the specific mechanisms involved in controlling the origin of biogenic and authigenic carbonates are still unclear. To address this knowledge gap, we analyzed core CSHC-4 sediment from the Okinawa Trough to examine the elemental and isotopic compositions of carbonates and their relationship to methane seepage and sea-level changes. Our results indicate that high-Mg calcite is the dominant authigenic carbonate, indicating moderate methane seep intensity. Negative carbon isotope values as low as −4.06‰ V-PDB of the bulk sediments deposited in the glacial period suggest a connection between the formation of authigenic carbonates and methane seepage. Negative oxygen isotope values as low as −2.6‰ V-PDB may be attributed to the input of 18O-depleted fluids influenced by gas hydrate formation. Biogenic carbonates contribute the majority (96.3%) of the total carbonate contents in sediments. Biogenic carbonate contents are lower during glacial periods and higher during interglacial periods. The reduced carbonate content during glacial periods may be due to lower export productivity influenced by the deepening of North Pacific Intermediate Water, as well as terrestrial inputs and anoxic conditions during low sea level periods. Our findings highlight the importance of considering both biogenic and authigenic carbonates when reconstructing paleoclimate and paleoceanography based on their geochemical characteristics. [ABSTRACT FROM AUTHOR]

Anaerobic oxidation of methane (AOM) is an important process that regulates methane budget in the global carbon cycle. Sulfate is traditionally regarded as the most important electron acceptor for AOM. However, recent studies reveal that reactive metal reduction-driven AOM (metal-AOM) may also present on natural environments. Partitioning the methane-C sink from anaerobic oxidation between sulfate reduction-driven AOM (sulfate-AOM) and metal-AOM is thus becoming a scientific challenge to be addressed. This study aimed to show that metal-AOM has a potential to complement sulfate-AOM, especially when methane seeps met sediments enriched in iron and manganese oxides supplied by hydrothermal plumes. Samples of authigenic carbonate were collected from the cold seeps on the western slope of the Okinawa Trough (OT), a semi-enclosed back-arc basin with cold seeps and hydrothermal activities coexist spatially. Petrologic and mineralogical observations provided faithful evidence of a close genetic relationship between goethite and authigenic carbonates, likely indicating the presence of metal-AOM although some contributions of organoclastic Fe reduction cannot be ruled out. The most possible place of metal-AOM was between the lower part of the sulfate–methane transition zone (SMTZ) and the immediate upper part of the methanogenic zone. The characteristics of δ13C carb [−53.7‰ to −3.3‰ Vienna-PeeDee Belemnite (VPDB)] also point to our carbonate samples as the products of AOM. These authigenic carbonates was further identified as three possible types of carbonate of different sources: sulfate-AOM, metal-AOM, and hydrothermal carbonates, depending on the correlations among concentrations of carbonate-associated sulfate (CAS), δ13C carb , and δ18O carb. Based on these findings, we tentatively suggested that the reduction of reactive metals carried by hydrothermal plumes might drive the methane oxidation in the adjacent cold seep areas, resulting in the precipitation of unique carbonates and enhancement the efficiency of "the benthic methane filter". This study reported the coupling or interaction between the two extreme submarine environments by metal-AOM for the first time, which might help in understanding and improving the global carbon and metal cycles now and in the past. • Three distinct types of carbonates exist in cold seeps in the Okinawa Trough. • Carbonate forms between lower part of SMTZ and upper part of methanogenic zone. • Hydrothermal has the potential to foster Fe-AOM in cold seep sediment. • Metal-AOM might have an influence on early Earth's methane flux and metal cycle. [ABSTRACT FROM AUTHOR]

Cold seep carbonate represents a faithful record of the ancient methane seepage and provides a nonnegligible contribution to the global carbon reservoir. On the western slope of the Northern Okinawa Trough (NOT), a recent seafloor visualized survey has discovered widespread crust of cold seep carbonate. Here we study mineralogy and geochemistry of these authigenic carbonate to investigate source origin and reconstruct its growth history. Mineralogically, the carbonate crusts are mainly composed of micritic aragonite, with botryoidal aragonite, framboidal pyrite, and microcrystalline authigenic gypsum. Petrographic characteristic unambiguously indicates that this carbonate precipitates in relatively open systems due to a considerable rate of sulfate-dependent anaerobic oxidation of methane (AOM). Regarding geochemistry, strongly 13C-depleted carbon isotope values (as low as −56.1‰, V-PDB) demonstrate that the carbon in the carbonate crusts is mainly derived from biogenic methane coupled with AOM. In contrast, the δ18O enrichment (up to +2.7‰, V-PDB) suggests that the fluid flow from which carbonate precipitated is sourced from dissociation of underlying natural gas hydrates. The U–Th ages of authigenic carbonates fall in the timescale of 22.8–55.7 ka BP, consistent with the period of sea-level lowstand in the late Pleistocene. Overall, several lines of evidence of this study indicate that extensive methane was released by gas hydrate decomposition during sea level fall, consequently resulting in the precipitations of carbonate crust in the NOT. Furthermore, the obviously episodic methane seepages led to the constant accretion from the interior to the exterior within the preformed crust, ultimately inducing the carbonate blocks, slabs and crusts to be exposed on the seafloor. The existence of large-scale carbonate crusts represents a good trapper of the later released carbon especially the isotopically light methane from the deep. • Aragonite is the dominated mineral phase in carbonate crust of Okinawa Trough. • Carbonate is sourced from gas hydrate and carbon mainly from biogenic methane. • U–Th age of carbonate crust is within the periods of sea-level lowstand. [ABSTRACT FROM AUTHOR]