Human activities and climate change are intensifying nitrogen loading, hypoxia, and salinity intrusion in estuarine systems, with important implications for nitrous oxide (N2O) emissions. However, the interactive effects of these co-occurring stressors on N2O production remain poorly understood. Here, we combined 15N-18O tracing and molecular analyses to investigate N2O production pathways and their microbial regulation in estuarine sediment based on a series of nitrogen-oxygen-salinity incubation treatments and field observations. Results showed that low salinity under weak hypoxia significantly increased the abundance of nirS and norB genes, indicating an enhanced potential for nitrite reduction to N2O, which in turn promoted N2O production, whereas high salinity mitigated this effect by suppressing Pseudomonas abundance. Nitrate input further stimulated denitrification, amplifying N2O production under weak hypoxia treatments. Heterotrophic denitrification was the major N2O production pathway overall, while under severe hypoxia, the contribution of nitrifier denitrification increased and could reach 65.57%. Elevated oxygen promoted complete nitrification, thereby reducing the contribution of the nitrifier nitrification and nitrifier denitrification pathways. In contrast, elevated salinity enhanced nitrifier denitrification and nitrification-coupled denitrification, associated with increased abundance of Nitrosomonas and Nitrospina. Notably, the low salinity and weak hypoxia zone emerged as a hotspot of N2O production, with a doubling of nitrogen input increasing production rates by approximately 78%. Overall, these findings demonstrate that nitrogen pollution, oxygen depletion, and salinity shifts interactively regulate N2O production in estuarine sediments, highlighting high-risk conditions for N2O emissions and providing insights for mitigating greenhouse gas emissions in human-impacted estuaries.
Archaea are single-celled microorganisms that are abundant in marine environments and play a key role in the carbon and nitrogen cycles. Archaea can biosynthesize a wide variety of isoprenoid membrane lipids, including isoprenoid glycerol dibiphytanyl glycerol tetraethers (isoGDGTs). Experimental and empirical evidence demonstrates that the number of cyclopentane moieties in isoGDGTs is related to growth temperature, leading to the formulation and development of the TEX86 ocean temperature proxy. The TEX86 proxy has been widely applied to marine sediments spanning the last 190 million years and has revealed unique insights into the evolution of ocean temperatures over diverse timescales. Other indices have been developed using archaeal lipids to reconstruct ecological and biogeochemical processes that operate within the marine realm. However, several knowledge gaps (e.g., depth of export production, non-temperature controls, application in non-analogue climates) limit the application of archaeal lipid-based proxies in modern and ancient marine environments. In this review, we critically assess the utility of archaeal lipids as tracers for (paleo) environmental change, with an emphasis on the TEX86 paleotemperature proxy.
Marine sediments host a vast deep biosphere, yet how microorganisms persist under severe energy limitation and govern long-term organic carbon (OC) preservation remains poorly understood. Here we show that archaea, primarily Bathyarchaeia, systematically displace bacteria with depth and form net growth zones across East China Sea shelf deep sediments. Multi-omics analyses and bioenergetic modelling reveal that this transition is driven by sustained archaeal metabolism of diverse recalcitrant OC compounds, and a physiological trade-off that prioritizes cellular maintenance over growth, minimizing mortality in deep sediments. This strategy triggers a fundamental shift in sedimentary carbon turnover: from rapid bacterial degradation of labile OC near the surface to persistent archaea-driven turnover of recalcitrant OC at depth. We estimate that Bathyarchaeia mediate ~77% of total OC degradation after 1,000 years of burial, corresponding to ~18% (~11.4 Pg C) of millennial OC degradation in global shelf sediments. These findings identify subsurface archaea as key microbial regulators of long-term OC preservation and reveal how physiological trade-offs sustain life and carbon turnover in the energy-limited deep biosphere.
Accurate reconstruction of paleo-ocean depths is essential for understanding the interplay between tectonic evolution and global climate change, yet existing methods face substantial limitations. Here, we assess the potential of glycerol dialkyl glycerol tetraethers (GDGTs)-archaeal lipid biomarkers-as a quantitative proxy for paleobathymetry. Analyzing a global dataset of marine surface sediments, we find that GDGT distributions exhibit systematic shifts with water depth. Using random forest machine learning models trained on combined isoGDGT and OH-GDGT profiles, we achieve high predictive performance (R2 = 0.85, RMSE = 646 m). Applying this approach to a 6-million-year sedimentary record from the northwest Australian Shelf reproduces key features captured by foraminifera-based reconstructions and reveals tectonically driven bathymetric evolution, including potential influences on the development of the Leeuwin Current. These results demonstrate the GDGT-based machine learning models offer a robust and effective framework for reconstructing paleo-ocean depths and probing the links between oceanography and tectonics.
ABSTRACT Methane oxidation coupled to sulfate reduction is the dominant process restricting methane release from cold seeps. Methane oxidation can also be coupled to nitrate/nitrite reduction, thereby linking the cycles of CH4, CO2, and N2O. However, how this coupling shifts during seep development and its impact on N2O production remains poorly understood. Here, we integrated geochemical profiling, 14C-based labeling, and omics-based analyses to quantify the process rates, identify the key microbial mediators, and assess the net N2O production across the developmental stages of cold seeps in the South China Sea. In an early-stage, polychaete-dominated seep, the depth-integrated, potential nitrate/nitrite-coupled methane oxidation rate reached 21.9 ± 3.0 mmol C/m2/day, accounting for 36%–73% of the total methane oxidation. By contrast, in a typical epifauna-prevalent mature seep, this contribution diminished to ~1% (0.62 ± 0.16 mmol C/m2/day), while sulfate-dependent methane oxidation became dominant. Omics data identified the predominant methane-oxidizing bacteria Methyloprofundus and QPIN01 (relative abundances of 7%–24%) as the potential mediators of nitrate/nitrite-coupled methane oxidation in the early-stage seep sediments. Consistent with the absence of N2O-reduction gene nosZ in these lineages, simultaneous nitrate and methane amendments significantly stimulated net N2O production by 14%–46% in the early-stage seep sediments. This increase correlated strongly with the potential nitrate/nitrite-coupled methane oxidation rate and was estimated to offset 41% ± 9% of the climate benefit gained through methane oxidation. These findings revealed the previously unrecognized successional dynamics of dominant methane oxidation pathways and necessitate the incorporation of nitrate/nitrite-coupled methane oxidation into assessments of greenhouse-gas release from these globally distributed ecosystems.IMPORTANCECold seep biota are widely regarded as a critical “biofilter” that restricts seafloor methane emission, mainly through coupled methane and sulfur cycling. This study refines this prevailing view by demonstrating a major shift in the dominant methane oxidation pathway during seep ecosystem development. Contrasting to the dominance of sulfate-coupled methane oxidation in mature seep systems, the early-stage seep is dominated by nitrate/nitrite-coupled methane oxidation, a process primarily mediated by methane-oxidizing bacteria. Crucially, these organisms possess a truncated denitrification pathway that leads to the production of nitrous oxide (N2O), a greenhouse gas with nearly 10 times the warming potential of methane. The resulting net N2O production thereby substantially offsets the climate benefit achieved by methane consumption. This study highlights the dual role of cold seep microbiota in regulating climate-active gases, underscoring that accurate assessment of their environmental impact requires a holistic understanding of temporal changes in coupled carbon and nitrogen cycles.
Hadal trenches, as key deep-sea environments for organic matter burial and microbial respiration, are therefore recognized hotspots for early diagenesis. Although phosphorus (P) cycling has been extensively studied in marginal sea sediments, its behavior in hadal trench sediments remains poorly understood. This study examines sedimentary P partitioning in the Kermadec Trench to identify the dominant controls on P speciation. Geochemical data reveal that P distribution is collectively influenced by redox conditions, organic matter content, and volcanic inputs. In the southern part of the trench, higher sedimentary TOC content directly enhances the preservation of iron-bound P (PFe, 21 % of total P) and organic P (Porg, 10 %). In contrast, northern sites, which are enriched in volcanic material (FeTOT up to 63.2 mg g-1), exhibit lower retention of reactive P (Prea, 40-45 %), likely due to Fe(III)-mediated dissimilatory iron reduction, along with higher volcanic silicate iron. This spatial heterogeneity exhibits variation influenced by hydrodynamic processes: deep western boundary currents carry terrigenous sediments northward, whereas surface currents distribute volcanic ash southward. Relative to continental shelves, hadal trenches display a greater predominance of detrital P burial (Pdetrital, 53 % of total P), as well as elevated proportions of iron-bound P (PFe,16 %) and authigenic apatite (Pauthi, 20 %). Our findings reveal volcanic activity as a critical control on phosphorus cycling in hadal systems, indicating that these environments are governed by a distinct set of biogeochemical processes.
Methylotrophic methanogenesis has recently been recognized as a key process driving cryptic methane cycling within sulfate‐reducing sediments. Here we conducted biogeochemical analyses of methanogenic substrates, activity, and communities in two sediment cores (4–5 m) from the East China Sea, to constrain the dynamics and controls of methylotrophic methanogenesis in coastal sediments. We detected micromolar concentrations of methane in the presence of sulfate and high methane concentrations (up to 4.2 mM) below the sulfate–methane transition zone (~ 150–170 cm). Stable isotope composition of methane was strongly depleted (−77‰ to −91‰), indicating its biological production. Methanogenic substrates including H 2 /CO 2 , acetate, and methylated compounds were detected in the porewaters and/or sediments. Radiotracer experiments indicated methane production from various substrates, and the presence of sulfate did not inhibit methanogenesis at either site. At the coastal site with the dominance of marine organic matter (total organic carbon: 0.6%; C/N ratio: ~ 6.4; δ 13 C‐total organic carbon: −22‰), methane was primarily produced from hydrogenotrophic methanogenesis, consistent with the progressive enrichment of 13 C in dissolved inorganic carbon with depth below the sulfate–methane transition zone. However, methylotrophic methanogenesis from methanol and trimethylamine contributed significantly to methane production (up to 30.2%) at the estuarine site (total organic carbon: 0.5%; C/N ratio: 7.4, δ 13 C‐total organic carbon: −23‰) with elevated terrestrial organic matter input, also reflected from the predominance of long chain odd carbon n‐alkanes. These findings suggested that organic carbon source and composition, instead of sulfate, control methanogenic activity, providing evidence that high terrestrial organic inputs could significantly enhance methylotrophic methanogenesis in coastal sediments.
Anthropogenic and climatic perturbations threaten to destabilize gas hydrates and release methane from its vast subseafloor reservoir. Yet the deep-sea ecosystem responses remain poorly understood. Our multi-year, in situ monitoring of a human-induced methane seep unveiled an exceptionally fast, de novo establishment of a methane-consuming ecosystem within 1-2 years, followed by a rapid succession toward natural mature seeps. Integrated biogeochemical and molecular analyses revealed an unexpectedly parallel proliferation of aerobic methanotrophs (Methyloprofundus), anaerobic methanotrophs (ANME-2e, ANME-3), and opportunistic fauna bioturbating the seabed to >50 cm depths. Within this intensively mixed zone, active animal-microbe interactions sustained rapid methane removal (30-60 mmol/m2/day) through intricate carbon, nitrogen, and sulfur redox coupling. Our work demonstrates that abrupt methane leakage can form an effective animal-microbe 'methane biofilter' far quicker than previously estimated, producing new insights into benthic natural mitigation capacity and limit that are critical for risk assessments and climate projections under increasing seabed methane efflux.
Abstract Branched glycerol dialkyl glycerol tetraethers (brGDGTs) are widely used as paleoclimate proxies on land, yet their origin in marine environments remains incompletely constrained. Here, we analyze suspended particulate matter collected from five depths at an open‐ocean station in the northern South China Sea and provide depth‐resolved evidence for substantial in situ brGDGT production within the oxic marine water column. BrGDGT concentrations show a pronounced subsurface maximum at ∼75 m and covary strongly with co‐occurring isoprenoid GDGTs, indicating that brGDGT synthesis is linked to marine microbial activity rather than being dominated by terrigenous supply alone. The brGDGT distributions are also distinct from those of terrestrial reference materials. These observations indicate that a significant fraction of marine brGDGTs can be produced well above the seafloor in oxic open‐ocean waters and they help constrain the ecological setting of the brGDGT signal ultimately exported to sediments.
Archaeal glycerol monoalkyl glycerol tetraethers (GMGTs) remain far less constrained than the widely used glycerol dialkyl glycerol tetraethers (GDGTs). We analyzed GMGTs in five sediment cores from the northern South China Sea spanning nearshore to deep-basin settings. GMGT-0 was detected only in the two nearshore cores and a reference Tibetan peat, whereas offshore South China Sea and East China Sea cores yielded no detectable GMGTs. Several nearly co-eluting compounds in marine sediments showed GDGT-like MS2 spectra, indicating that GMGT assignments require more than retention-time agreement. In nearshore cores, GMGT abundance covaries with delta C-13(TOC) and TOC/TN, and these relationships strengthen after normalization to crenarchaeol (GMGTs/CREN). Together, these observations support a predominantly terrestrial source for the detected GMGTs and suggest that, with careful chromatographic and spectral verification, GMGTs/CREN may provide a complementary tracer of terrestrial organic matter input to marine sediments.
In this research, aberration-corrected high-angle annular dark-field scanning transmission electron microscopy (HADDF-STEM) and first-principles calculations are utilized to investigate the Cu-containing (3" precipitation phase in Al-Mg-Si-Cu alloys. The occupancy of Cu atoms and its influence on structural, mechanical and electronic properties are analyzed. The findings reveal that Cu atoms can occupy specific sites in the (3" phase, with Mg5AlCuSi4 exhibiting the highest thermodynamic stability. The elastic constants affirm the mechanical stability of all (3" phase structures. Moreover, the addition of Cu modifies the mechanical properties, resulting in a significant alteration in the modulus of elasticity and an increase in elastic anisotropy, especially Mg4Al2CuSi4 showcases excellent mechanical properties and the strongest anisotropy. The alloys demonstrate metallic properties and the presence of covalent-like bonds between Si and Cu atoms. In this study, a combination of experimental and theoretical analyses verified that Mg4+xAl2-xCuSi4 is the most stable configuration for the Cucontaining (3" phase, providing insights into the properties of Al-Mg-Si-Cu alloys and ideas for subsequent development of advanced aluminium alloys.
Globally, vast amounts of methane are trapped within subseafloor gas hydrates1. Recent evidence suggests that climate- and human-induced perturbations can destabilize gas hydrates and trigger methane release2-5, yet the response of deep-sea ecosystems to these changes remains poorly understood. Here we show multi-year in situ monitoring of seabed ecosystem following methane leakage induced by hydrate exploration activities. Within just two years, benthic microbial and eukaryotic diversity in the affected areas declined significantly, while microbial and macrofaunal abundance increased. Integrated geochemical and omics analyses reveal the rapid successional shift of seabed ecosystem to a novel chemosynthetic system. Aerobic methanotrophs (Methyloprofundus) co-established with unexpectedly fast growing anaerobic methanotrophic archaea (ANME-3), accompanied by a rapid recruitment of opportunistic polychaetes that bioirrigated the seabed to >50 cm depths. The active animal-microbe interactions sustained exceptionally high rates of methane oxidation that utilized diverse electron acceptors. We demonstrate that methane hydrate destabilization can trigger rapid collapse of native seabed ecosystem while driving the formation of an effective "methane biofilter" consuming this potent greenhouse gas much faster than previously estimated. Understanding seabed ecosystem response and feedback is critical for predicting benthic methane cycling under ongoing global change and for developing sustainable strategies for methane hydrate resource management.
Hadal trenches are critical hotspots for organic carbon (OC) deposition and diagenesis, yet the mechanisms controlling carbon sequestration, particularly the role of episodic tectonic and volcanic events, remain poorly constrained. This study integrates geochemical analyses of solid sediments and porewater from sediment cores collected at six stations along two transects in the Kermadec Trench to characterize OC sources, transport, and mineralization dynamics within this hadal trench system. Our results reveal a distinct south-to-north sediment transport pattern along the trench axis, leading to an accumulation of marine-derived OC in the south and terrestrial OC in the north. Importantly, earthquake-triggered turbidity currents in the central trench and volcanic eruptions in the north dominate episodic disturbances, exerting primary control over sediment deposition and diagenesis. These downslope currents transport significant OC fluxes from continental slopes to trench axes, enhancing burial rates 20-fold relative to steady-state sedimentation and promoting OC preservation in axial domains. Our findings demonstrate that spatial heterogeneity in hadal carbon cycling is primarily governed by episodic geological events, providing essential insights for accurate quantification of carbon fluxes and their integration into global biogeochemical models.
Marine sediment is Earth’s largest reservoir of organic carbon and harbors >50% of the microbial cells in the ocean. Whether the organic carbon deposited to seabed is mineralized back to CO2 or preserved over geological timescale, is largely controlled by the microbial processes occurring at sediment-water interface and those key geochemical transition zones below the seafloor. Despite the intimate connection of sediment microbes to Earth’s carbon cycle, the mechanisms, fluxes, and ecological effects of the microbially driven carbon transformation processes in marine sediments, as well as their potential contributions to climate change and mitigation, remain largely unsolved. To this end, we propose the conceptual framework MCT-S (Microbially driven Carbon Transformation in marine Sediments) to guide the understanding and research on sediment carbon cycles. Under the guidance of MCT-S, we integrated interdisciplinary techniques of geochemistry, microbiology, molecular ecology, mathematical modeling, environment simulation as well as designing and fabricating in situ process measuring instruments, to resolve the mechanisms and quantify the contributions of microbial processes in benthic carbon cycling. Our recent studies revealed novel microbial lineages, metabolisms, and/or interplays that are involved in the degradation of refractory organic macromolecules (e.g. lignin, long-chain alkanes), the production and consumption of methane, and the cycling of iron-bound organic carbon at seafloor. These advances produce insights that are necessary to understand the inner workings of carbon cycle at and below the sediment-water interface, underpinning the foundation for elucidating the potential responses and contributions of seafloor microbes to climate change and the related oceanic mitigation actions.
Bathyarchaeia, an abundant and ecologically versatile archaea found commonly in marine sediments, has a key role in the global carbon cycle. However, its lipid biomarkers and carbon assimilation mechanisms are poorly understood. Here, using a highly enriched Bathyarchaeia culture (>95% archaea) obtained from estuarine sediment of the East China Sea, we show that Baizosediminiarchaeum (formerly subgroup Bathy-8), the most abundant and widespread Bathyarchaeia group on Earth, synthesizes butanetriol dialkyl glycerol tetraethers (BDGTs) as its dominant membrane lipids. BDGTs are unusual archaeal tetraether lipids characterized by a butanetriol backbone instead of the typical glycerol, challenging fundamental assumptions in archaeal lipid biochemistry. Although BDGTs have been previously identified in the methanogen Methanomassiliicoccus luminyensis, we now provide direct evidence that Bathyarchaeia also synthesizes BDGTs, definitively establishing this globally abundant group as a natural BDGT producer. Stable isotope probing with 13C-bicarbonate shows that Baizosediminiarchaeum assimilates carbon into BDGTs from both inorganic carbon and lignin. These unique carbon assimilation strategies suggest the biogeochemical importance of Baizosediminarchaeum in marine carbon cycling and organic matter decomposition.
Petroleum hydrocarbons are traditional pollutants in coastal sedimentary environments, and the concentration of total petroleum hydrocarbons (TPH) has been used as a proxy to assess oil contamination in sediments. In this study, we investigated the distribution of TPH and n-alkanes (n-C14—n-C34) along two ca. 4 m sediment cores from the East China Sea (ECS) and further analyzed the n-alkane-based diagnostic parameters. The TPH concentrations (7.7–21.7 μg/g, with an outlier of 60.3 μg/g) indicated slight petroleum pollution at both sites. Among the hydrocarbons, higher abundances were observed for long-chain n-alkanes n-C29, n-C31 and n-C33. The terrestrial n-alkanes accounted for 25
Inward membrane budding, i.e., the bending of membrane towards the cytosol, is essential for forming and maintaining eukaryotic organelles. In eukaryotes, Arf GTPases initiate this inward budding. Our research shows that Asgard archaea genomes encode putative Arf proteins (AArfs). AArfs possess structural elements characteristic of their eukaryotic counterparts. When expressed in yeast and mammalian cells, some AArfs displayed GTP-dependent membrane targeting. In vitro, AArf associated with both eukaryotic and archaeal membranes. In yeast, AArfs interacted with and were regulated by key organelle biogenesis players. Expressing an AArf led to a massive proliferation of endomembrane organelles including the endoplasmic reticulum and Golgi. This AArf interacted with Sec23, a COPII vesicle coat component, in a GTP-dependent manner. These findings suggest certain AArfs are membrane-associating molecular switches with the functional potential to initiate organelle biogenesis, and the evolution of a functional coat could be the next critical step towards establishing eukaryotic cell architecture.
Glycerol dialkyl glycerol tetraethers (GDGTs), membrane lipids produced by archaea, have been widely utilized as biomarkers for paleotemperature reconstructions. While the relationship between GDGTs and temperature adaptation has been studied, the effects of structural modifications, specifically cyclopentane and cyclohexane rings, on membrane properties remains insufficiently understood. In this study, molecular dynamics simulations were employed to examine how these structural modifications influence GDGT membrance fluidity, with an emphasis on high-temperature adaptation in archaea. Our results demonstrate that an increasing number of cyclopentane rings is assoicated with reduced membrane fluidity, highlighting their role in facilitating hightemperature acclimation. Additionally, cyclohexane modifications in crenarchaeol, along with its isomerization, further reduce membrane fluidity. These findings indicate a clear link between lipid cyclization and thermal adaptation in archaea. Furthermore, the significant differences in membrane fluidity between GDGT-1 and GDGT-2 are consistent with the theoretical basis of the TEX86 temperature proxy. Interestingly, while the cyclohexane modification of crenarchaeol in environmental samples suggests cold adaptation, this observation contrasts to findings from culture data and molecular dynamic simulations, suggesting the influence of additional factors. Based on these insights, we propose a novel sea surface temperatures reconstruction metric, TEX86MD, which enhances the accuracy of the TEX86 proxy, and provides broader global applicability, especially in the polar regions.
Tetraether membrane lipid glycerol dialkyl glycerol tetraether (GDGT) is a characteristic lipid of archaea that contributes to adaptation to a variety of environments and has been widely used in ecological and geochemical studies. Alkyl-chain methyl-modified GDGTs (Me-GDGTs) as one important component have been detected in both environmental and culture samples. However, the effect of methyl modification on archaeal membrane lipids remains unclear, hampering the development of environmental proxies based on the exact understanding of the underlying mechanism. Here, we reveal the perturbation of molecular order by methyl modification through molecular dynamics simulations, showing that methyl modification can increase membrane fluidity, explaining that this is a form of low-temperature acclimation. This hypothesis was also validated in environmental samples. This study reveals the role of methyl modifications in low-temperature adaptation in archaea, expanding that hydrophobic carbon chain methylation has unified physiological significance in three domain life. Our study highlights the role of molecular dynamics simulations in the development of lipid biomarkers, provides new insights into the mechanisms of temperature adaptation in microorganisms, and lays the groundwork for the development of new environmental proxies.
The long-term burial of organic carbon in marginal seas plays a critical role in Earth’s carbon cycle and climate change. However, the mechanism of organic carbon (OC) burial in the Okinawa Trough (OT) during glacial-interglacial timescales remains unclear. In this study, we analyzed the foraminiferal carbon isotopes, total organic carbon (TOC), and δ13C-TOC over the past 200 ka in core Z1 collected in the central OT. We aimed to reveal the history of OC burial in the middle Okinawa Trough during the past 200 ka, and we combined our findings with relevant paleoenvironmental indices to reveal underlying mechanisms. We found reduced surface primary productivity during MIS 6, which may indicate changes in the pathways of the Kuroshio Current (KC). Furthermore, we observed decoupling between high TOC flux and low OC burial during glacial periods. We proposed that the dilution effect caused by the high sedimentation rate and poor OC preservation during the glacial period resulted in the low TOC content. Ventilation of the North Pacific Intermediate Water (NPIW) regulated the redox conditions of the intermediate water in the Okinawa Trough. Additionally, the intensified Kuroshio Current during interglacial phases led to water column stratification, creating reducing conditions in the bottom water and facilitating improved OC preservation. Subsequently, the enhanced water column oxygenation resulting from the oxygen carried by the intensified glacial NPIW weakened the burial of OC. This study sheds new light on our understanding of the carbon cycle in marginal seas on a glacial-interglacial timescale.