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Microbially mediated nitrogen cycling in carbon-dominated cold seep environments remains poorly understood. So far anaerobic methanotrophic archaea (ANME-2) and their sulfate-reducing bacterial partners (SEEP-SRB1 clade) have been identified as diazotrophs in deep sea cold seep sediments. However, it is unclear whether other microbial groups can perform nitrogen fixation in such ecosystems. To fill this gap, we analyzed 61 metagenomes, 1428 metagenome-assembled genomes, and six metatranscriptomes derived from 11 globally distributed cold seeps. These sediments contain phylogenetically diverse nitrogenase genes corresponding to an expanded diversity of diazotrophic lineages. Diverse catabolic pathways were predicted to provide ATP for nitrogen fixation, suggesting diazotrophy in cold seeps is not necessarily associated with sulfate-dependent anaerobic oxidation of methane. Nitrogen fixation genes among various diazotrophic groups in cold seeps were inferred to be genetically mobile and subject to purifying selection. Our findings extend the capacity for diazotrophy to five candidate phyla (Altarchaeia, Omnitrophota, FCPU426, Caldatribacteriota and UBA6262), and suggest that cold seep diazotrophs might contribute substantially to the global nitrogen balance. Microbial nitrogen fixation could be important in the deep sea. Here the authors investigate metagenomes and metatranscriptomes of diazotrophs from deep sea cold seep sediments, reveal greater phylogenetic and functional diversity than hitherto known.

In marine ecosystems, viruses exert control on the composition and metabolism of microbial communities, influencing overall biogeochemical cycling. Deep sea sediments associated with cold seeps are known to host taxonomically diverse microbial communities, but little is known about viruses infecting these microorganisms. Here, we probed metagenomes from seven geographically diverse cold seeps across global oceans to assess viral diversity, virus–host interaction, and virus-encoded auxiliary metabolic genes (AMGs). Gene-sharing network comparisons with viruses inhabiting other ecosystems reveal that cold seep sediments harbour considerable unexplored viral diversity. Most cold seep viruses display high degrees of endemism with seep fluid flux being one of the main drivers of viral community composition. In silico predictions linked 14.2% of the viruses to microbial host populations with many belonging to poorly understood candidate bacterial and archaeal phyla. Lysis was predicted to be a predominant viral lifestyle based on lineage-specific virus/host abundance ratios. Metabolic predictions of prokaryotic host genomes and viral AMGs suggest that viruses influence microbial hydrocarbon biodegradation at cold seeps, as well as other carbon, sulfur and nitrogen cycling via virus-induced mortality and/or metabolic augmentation. Overall, these findings reveal the global diversity and biogeography of cold seep viruses and indicate how viruses may manipulate seep microbial ecology and biogeochemistry.

Phosphorus is essential for life and critically influences marine productivity. Despite geochemical evidence of active phosphorus cycling in deep-sea cold seeps, the microbial processes involved remain poorly understood. Traditional sequence-based searches often fail to detect proteins with remote homology. To address this, we developed a deep learning model, LucaPCycle, integrating raw sequences and contextual embeddings based on the protein language model ESM2-3B. LucaPCycle identified 5241 phosphorus-cycling protein families from global cold seep gene and genome catalogs, substantially enhancing our understanding of their diversity, ecology, and function. Among previously unannotated sequences, we discovered three alkaline phosphatase families that feature unique domain organizations and preserved enzymatic capabilities. These results highlight previously overlooked ecological importance of phosphorus cycling within cold seeps, corroborated by data from porewater geochemistry, metatranscriptomics, and metabolomics. We revealed a previously unrecognized diversity of archaea, including Asgardarchaeota, anaerobic methanotrophic archaea and Thermoproteota, which contribute to organic phosphorus mineralization and inorganic phosphorus solubilization through various mechanisms. Additionally, auxiliary metabolic genes of cold seep viruses primarily encode the PhoR-PhoB regulatory system and PhnCDE transporter, potentially enhancing their hosts’ phosphorus utilization. Overall, LucaPCycle are capable of accessing previously ‘hidden’ sequence spaces for microbial phosphorus cycling and can be applied to various ecosystems. The microbial processes involved in deep sea phosphorous cycling are unclear. Here, the authors develop a deep learning model, LucaPCycle, identifying alkaline phosphatase families and archaea that contribute to phosphorous cycling in deep sea cold seeps.

Arsenic accumulation in seafloor cold seeps is poorly understood. Here, we investigate the interplay between arsenic and methane biogeochemical cycles at the Haima cold seep, South China Sea. Geochemical analyses showed elevated arsenic levels in seep sediments, primarily as sulfide‐bound forms, with strong correlations between dissolved arsenic and methane oxidation proxies (DIC, R2 = 0.64, p < 0.05; δ13CDIC, R2 = 0.86, p < 0.05). Metagenomic sequencing revealed diverse functional genes related to arsenic‐, methane‐ and sulfur cycling, including co‐occurrence of arrA and dsrA in sulfate‐reducing bacteria Desulfobacterota, which are symbionts of Anaerobic Methane Oxidizing Archaea. We propose that anaerobic oxidation of methane (AOM) and the enhanced “metal particle shuttle effect,” both associated with methane release, drive arsenic sequestration. Cold seeps may sequester 0.04–1.81 × 103 kg arsenic annually. These finding highlights cold seeps are hotspots of arsenic cycling with implications for oceanic arsenic chemistry.

Background Gas hydrate-bearing subseafloor sediments harbor a large number of microorganisms. Within these sediments, organic matter and upward-migrating methane are important carbon and energy sources fueling a light-independent biosphere. However, the type of metabolism that dominates the deep subseafloor of the gas hydrate zone is poorly constrained. Here we studied the microbial communities in gas hydrate-rich sediments up to 49 m below the seafloor recovered by drilling in the South China Sea. We focused on distinct geochemical conditions and performed metagenomic and metatranscriptomic analyses to characterize microbial communities and their role in carbon mineralization. Results Comparative microbial community analysis revealed that samples above and in sulfate-methane interface (SMI) zones were clearly distinguished from those below the SMI. Chloroflexota were most abundant above the SMI, whereas Caldatribacteriota dominated below the SMI. Verrucomicrobiota, Bathyarchaeia, and Hadarchaeota were similarly present in both types of sediment. The genomic inventory and transcriptional activity suggest an important role in the fermentation of macromolecules. In contrast, sulfate reducers and methanogens that catalyze the consumption or production of commonly observed chemical compounds in sediments are rare. Methanotrophs and alkanotrophs that anaerobically grow on alkanes were also identified to be at low abundances. The ANME-1 group actively thrived in or slightly below the current SMI. Members from Heimdallarchaeia were found to encode the potential for anaerobic oxidation of short-chain hydrocarbons. Conclusions These findings indicate that the fermentation of macromolecules is the predominant energy source for microorganisms in deep subseafloor sediments that are experiencing upward methane fluxes. 84_GYpCEs37AndHmKLQLsZ Video Abstract

Cold seeps harbor abundant and diverse microbes with tremendous potential for biological applications and that have a significant influence on biogeochemical cycles. Although recent metagenomic studies have expanded our understanding of the community and function of seep microorganisms, knowledge of the diversity and genetic repertoire of global seep microbes is lacking. Here, we collected a compilation of 165 metagenomic datasets from 16 cold seep sites across the globe to construct a comprehensive gene and genome catalog. The non-redundant gene catalog comprised 147 million genes, and 36% of them could not be assigned to a function with the currently available databases. A total of 3,164 species-level representative metagenome-assembled genomes (MAGs) were obtained, most of which (94%) belonged to novel species. Of them, 81 ANME species were identified that cover all subclades except ANME-2d, and 23 syntrophic SRB species spanned the Seep-SRB1a, Seep-SRB1g, and Seep-SRB2 clades. The non-redundant gene and MAG catalog is a valuable resource that will aid in deepening our understanding of the functions of cold seep microbiomes.

Cold seeps, where cold hydrocarbon-rich fluid escapes from the seafloor, show strong enrichment of toxic metalloid arsenic (As). The toxicity and mobility of As can be greatly altered by microbial processes that play an important role in global As biogeochemical cycling. However, a global overview of genes and microbes involved in As transformation at seeps remains to be fully unveiled. Using 87 sediment metagenomes and 33 metatranscriptomes derived from 13 globally distributed cold seeps, we show that As detoxification genes ( arsM , arsP , arsC1 / arsC 2, acr3 ) were prevalent at seeps and more phylogenetically diverse than previously expected. Asgardarchaeota and a variety of unidentified bacterial phyla (e.g. 4484-113, AABM5-125-24 and RBG-13-66-14) may also function as the key players in As transformation. The abundances of As cycling genes and the compositions of As-associated microbiome shifted across different sediment depths or types of cold seep. The energy-conserving arsenate reduction or arsenite oxidation could impact biogeochemical cycling of carbon and nitrogen, via supporting carbon fixation, hydrocarbon degradation and nitrogen fixation. Overall, this study provides a comprehensive overview of As cycling genes and microbes at As-enriched cold seeps, laying a solid foundation for further studies of As cycling in deep sea microbiome at the enzymatic and processual levels.

The effect of seafloor cold seeps on the biogeochemical cycling of mercury (Hg) remains enigmatic. Here we demonstrate substantial enrichments of mercury and methylmercury, along with the presence of microbes capable of metabolizing mercury in sediments of the Haima cold seep, South China Sea, by analyzing mercury and methylmercury concentrations, mercury isotopic composition analyses and metagenomic analyses of sediment cores. Compared to the reference area, the sediments in the upper sediment column of the active-seep area were 2.4 times enriched in Hg and 10.5 times in methylmercury. The slope of the capital delta ratio of mercury 199 to mercury 201 (Δ 199 Hg/Δ 201 Hg) with 1.23 ± 0.10 in the active-seep area indicate the occurrence of dark redox reactions. Genes related to mercury methylation ( hgcA ), demethylation ( merB ) and reduction ( merA ) were phylogenetically associated with several bacterial and archaeal linages. We roughly estimated an additional 2,835 Mg mercury and 9 Mg methylmercury are stored in cold seep globally. In summary, we propose that cold seeps globally function as a previously unrecognized sink for mercury and source for methylmercury in the deep ocean.

ABSTRACT The seafloor sulfide structures of inactive vents are known to host abundant and diverse microorganisms potentially supported by mineralogy of sulfides. However, little is known about the diversity and distribution of microbial functions. Here, we used genome-resolved metagenomics to predict microbial metabolic functions and the contribution of horizontal gene transfer to the functionality of microorganisms inhabiting several hydrothermally inactive seafloor deposits among globally distributed deep-sea vent fields. Despite of geographically distant vent fields, similar microbial community patterns were observed with the dominance of Gammaproteobacteria, Bacteroidota and previously overlooked Candidatus Patescibacteria. Metabolically flexible Gammaproteobacteria are major potential primary producers utilizing mainly sulfur, iron and hydrogen as electron donors coupled with oxygen and nitrate respiration for chemolithoautotrophic growth. In addition to heterotrophic microorganisms like free-living Bacteroidota, Ca. Patescibacteria potentially perform fermentative recycling of organic carbon. Finally, we provided evidence that many functional genes that are central to energy metabolism have been laterally transferred among members within the community and largely within the same class. Taken together, these findings shed light on microbial ecology and evolution in inactive seafloor sulfide deposits after the cessation of hydrothermal activities. Inactive seafloor sulfide deposits harbor diverse microbial functional genes with potential contribution of horizontal gene transfer.

Du, P.; Zhang, C., and Yang, L., 2020. The impact of perceived value and group norm on environmentally friendly behavior of mangrove reserves in coastal cities: The mediating role of tourism satisfaction. In: Liu, X. and Zhao, L. (eds.), Today's Modern Coastal Society: Technical and Sociological Aspects of Coastal Research. Journal of Coastal Research, Special Issue No. 111, pp. 243–247. Coconut Creek (Florida), ISSN 0749-0208. With the rapid development of China's coastal cities, mangrove conservation faces various environmental influences brought on by the thousands of visitors. This study proposes the hypothesis that latent variables such as environmental knowledge, perceived value, group norms, and satisfaction have significant positive effects on environmentally friendly behavior and refine influencing aspects and paths. The Mangrove Nature Reserve of Shenzhen is used as the study area, and the following model analysis results are found: (1) Perceived value contributes the most to environmentally friendly behavior, (2) group norms have the second-greatest effect on environmentally friendly behavior, which indicates that tourists in the same group are easily affected by the people around them; and (3) tourism satisfaction mediates the relationship between environmental knowledge and environmentally friendly behavior. The findings could help managers of mangrove conservation recognize the paths for influencing environmentally friendly behavior and improve the level of environmental management and tourism services.