Potential coupling of microbial methane, nitrogen, and sulphur cycling in the Okinawa Trough cold seep sediments.

The Okinawa Trough (OT) is a back-arc basin with a wide distribution of active cold seep systems. However, our understanding of the metabolic function of microbial communities in the cold seep sediments of the OT remains limited. In this study, we investigated the vertical profiles of functional genes involved in methane, nitrogen, and sulphur cycling in the cold seep sediments of the OT. Furthermore, we explored the possible coupling mechanisms between these biogeochemical cycles. The study revealed that the majority of genes associated with the nitrogen and sulphur cycles were most abundant in the surface sediment layers. However, only the key genes responsible for sulphur disproportionation (sor), nitrogen fixation (nifDKH), and methane metabolism (mcrABG) were more prevalent within sulfate-methane transition zone (SMTZ). Significant positive correlations (P < 0.05) were observed between functional genes involved in sulphur oxidation, thiosulphate disproportionation with denitrification, and dissimilatory nitrate reduction to ammonium (DNRA), as well as between AOM/methanogenesis and nitrogen fixation, and between sulphur disproportionation and AOM. A genome of Filomicrobium (class Alphaproteobacteria) has demonstrated potential in chemoautotrophic activities, particularly in coupling DNRA and denitrification with sulphur oxidation. Additionally, the characterized sulfate reducers such as Syntrophobacterales have been found to be capable of utilizing nitrate as an electron acceptor. The predominant methanogenic/methanotrophic groups in the OT sediments were identified as H2-dependent methylotrophic methanogens (Methanomassiliicoccales and Methanofastidiosales) and ANME-1a. This study offered a thorough understanding of microbial ecosystems in the OT cold seep sediments, emphasizing their contribution to nutrient cycling.IMPORTANCEThe Okinawa Trough (OT) is a back-arc basin formed by extension within the continental lithosphere behind the Ryukyu Trench arc system. Cold seeps are widespread in the OT. While some studies have explored microbial communities in OT cold seep sediments, their metabolic potential remains largely unknown. In this study, we used metagenomic analysis to enhance comprehension of the microbial community's role in nutrient cycling and proposed hypotheses on the coupling process and mechanisms involved in biogeochemical cycles. It was revealed that multiple metabolic pathways can be performed by a single organism or microbes that interact with each other to carry out various biogeochemical cycling. This data set provided a genomic road map on microbial nutrient cycling in OT sediment microbial communities.

Unveiling unique microbial nitrogen cycling and nitrification driver in coastal Antarctica.

Largely removed from anthropogenic delivery of nitrogen (N), Antarctica has notably low levels of nitrogen. Though our understanding of biological sources of ammonia have been elucidated, the microbial drivers of nitrate (NO3-) cycling in coastal Antarctica remains poorly understood. Here, we explore microbial N cycling in coastal Antarctica, unraveling the biological origin of NO3- via oxygen isotopes in soil and lake sediment, and through the reconstruction of 1968 metagenome-assembled genomes from 29 microbial phyla. Our analysis reveals the metabolic potential for microbial N2 fixation, nitrification, and denitrification, but not for anaerobic ammonium oxidation, signifying a unique microbial N-cycling dynamic. We identify the predominance of complete ammonia oxidizing (comammox) Nitrospira, capable of performing the entire nitrification process. Their adaptive strategies to the Antarctic environment likely include synthesis of trehalose for cold stress, high substrate affinity for resource utilization, and alternate metabolic pathways for nutrient-scarce conditions. We confirm the significant role of comammox Nitrospira in the autotrophic, nitrification process via 13C-DNA-based stable isotope probing. This research highlights the crucial contribution of nitrification to the N budget in coastal Antarctica, identifying comammox Nitrospira clade B as a nitrification driver.

Diversity and potential host-interactions of viruses inhabiting deep-sea seamount sediments.

Seamounts are globally distributed across the oceans and form one of the major oceanic biomes. Here, we utilized combined analyses of bulk metagenome and virome to study viral communities in seamount sediments in the western Pacific Ocean. Phylogenetic analyses and the protein-sharing network demonstrate extensive diversity and previously unknown viral clades. Inference of virus-host linkages uncovers extensive interactions between viruses and dominant prokaryote lineages, and suggests that viruses play significant roles in carbon, sulfur, and nitrogen cycling by compensating or augmenting host metabolisms. Moreover, temperate viruses are predicted to be prevalent in seamount sediments, which tend to carry auxiliary metabolic genes for host survivability. Intriguingly, the geographical features of seamounts likely compromise the connectivity of viral communities and thus contribute to the high divergence of viral genetic spaces and populations across seamounts. Altogether, these findings provides knowledge essential for understanding the biogeography and ecological roles of viruses in globally widespread seamounts.

A vast repertoire of secondary metabolites potentially influences community dynamics and biogeochemical processes in cold seeps.

In deep-sea cold seeps, microbial communities thrive on the geological seepage of hydrocarbons and inorganic compounds, differing from photosynthetically driven ecosystems. However, their biosynthetic capabilities remain largely unexplored. Here, we analyzed 81 metagenomes, 33 metatranscriptomes, and 7 metabolomes derived from nine different cold seep areas to investigate their secondary metabolites. Cold seep microbiomes encode diverse and abundant biosynthetic gene clusters (BGCs). Most BGCs are affiliated with understudied bacteria and archaea, including key mediators of methane and sulfur cycling. The BGCs encode diverse antimicrobial compounds that potentially shape community dynamics and various metabolites predicted to influence biogeochemical cycling. BGCs from key players are widely distributed and highly expressed, with their abundance and expression levels varying with sediment depth. Sediment metabolomics reveals unique natural products, highlighting uncharted chemical potential and confirming BGC activity in these sediments. Overall, these results demonstrate that cold seep sediments serve as a reservoir of hidden natural products and sheds light on microbial adaptation in chemosynthetically driven ecosystems.

Distinct microbial hydrogen and reductant disposal pathways explain interbreed variations in ruminant methane yield.

Ruminants are essential for global food security, but these are major sources of the greenhouse gas methane. Methane yield is controlled by the cycling of molecular hydrogen (H2), which is produced during carbohydrate fermentation and is consumed by methanogenic, acetogenic, and respiratory microorganisms. However, we lack a holistic understanding of the mediators and pathways of H2 metabolism and how this varies between ruminants with different methane-emitting phenotypes. Here, we used metagenomic, metatranscriptomic, metabolomics, and biochemical approaches to compare H2 cycling and reductant disposal pathways between low-methane-emitting Holstein and high-methane-emitting Jersey dairy cattle. The Holstein rumen microbiota had a greater capacity for reductant disposal via electron transfer for amino acid synthesis and propionate production, catalyzed by enzymes such as glutamate synthase and lactate dehydrogenase, and expressed uptake [NiFe]-hydrogenases to use H2 to support sulfate and nitrate respiration, leading to enhanced coupling of H2 cycling with less expelled methane. The Jersey rumen microbiome had a greater proportion of reductant disposal via H2 production catalyzed by fermentative hydrogenases encoded by Clostridia, with H2 mainly taken up through methanogenesis via methanogenic [NiFe]-hydrogenases and acetogenesis via [FeFe]-hydrogenases, resulting in enhanced methane and acetate production. Such enhancement of electron incorporation for metabolite synthesis with reduced methanogenesis was further supported by two in vitro measurements of microbiome activities, metabolites, and public global microbiome data of low- and high-methane-emitting beef cattle and sheep. Overall, this study highlights the importance of promoting alternative H2 consumption and reductant disposal pathways for synthesizing host-beneficial metabolites and reducing methane production in ruminants.

Deep-sea microbial genetic resources: new frontiers for bioprospecting.

Deep-sea ecosystems are home to a diverse community of microorganisms. These microbes are not only fundamental to ecological processes but also a treasure trove of natural products and enzymes with significant scientific and industrial applications. This forum focuses on the vast diversity of deep-sea microbes and their potential for bioprospecting. It also discusses threats posed by climate change and deep-sea mining to deep-sea microbial genetic resources, and proposes future research directions.

A comprehensive genomic catalog from global cold seeps.

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.

Viruses in deep-sea cold seep sediments harbor diverse survival mechanisms and remain genetically conserved within species.

Deep sea cold seep sediments have been discovered to harbor novel, abundant, and diverse bacterial and archaeal viruses. However, little is known about viral genetic features and evolutionary patterns in these environments. Here, we examined the evolutionary ecology of viruses across active and extinct seep stages in the area of Haima cold seeps in the South China Sea. A total of 338 viral operational taxonomic units are identified and linked to 36 bacterial and archaeal phyla. The dynamics of host-virus interactions are informed by diverse antiviral defense systems across 43 families found in 487 microbial genomes. Cold seep viruses are predicted to harbor diverse adaptive strategies to persist in this environment, including counter-defense systems, auxiliary metabolic genes, reverse transcriptases, and alternative genetic code assignments. Extremely low nucleotide diversity is observed in cold seep viral populations, being influenced by factors including microbial host, sediment depth, and cold seep stage. Most cold seep viral genes are under strong purifying selection with trajectories that differ depending on whether cold seeps are active or extinct. This work sheds light on the understanding of environmental adaptation mechanisms and evolutionary patterns of viruses in the sub-seafloor biosphere.

The majority of microorganisms in gas hydrate-bearing subseafloor sediments ferment macromolecules.

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. Video Abstract.

Unexpected genetic and microbial diversity for arsenic cycling in deep sea cold seep sediments.

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/arsC2, 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.

Metal-Driven Anaerobic Oxidation of Methane as an Important Methane Sink in Methanic Cold Seep Sediments.

Anaerobic oxidation of methane (AOM) coupled with reduction of metal oxides is supposed to be a globally important bioprocess in marine sediments. However, the responsible microorganisms and their contributions to methane budget are not clear in deep sea cold seep sediments. Here, we combined geochemistry, muti-omics, and numerical modeling to study metal-dependent AOM in methanic cold seep sediments in the northern continental slope of the South China Sea. Geochemical data based on methane concentrations, carbon stable isotope, solid-phase sediment analysis, and pore water measurements indicate the occurrence of anaerobic methane oxidation coupled to metal oxides reduction in the methanic zone. The 16S rRNA gene and transcript amplicons, along with metagenomic and metatranscriptomic data suggest that diverse anaerobic methanotrophic archaea (ANME) groups actively mediated methane oxidation in the methanic zone either independently or in syntrophy with, e.g., ETH-SRB1, as potential metal reducers. Modeling results suggest that the estimated rates of methane consumption via Fe-AOM and Mn-AOM were both 0.3 µmol cm-2 year-1, which account for ~3% of total CH4 removal in sediments. Overall, our results highlight metal-driven anaerobic oxidation of methane as an important methane sink in methanic cold seep sediments. IMPORTANCE Anaerobic oxidation of methane (AOM) coupled with reduction of metal oxides is supposed to be a globally important bioprocess in marine sediments. However, the responsible microorganisms and their contributions to methane budget are not clear in deep sea cold seep sediments. Our findings provide a comprehensive view of metal-dependent AOM in the methanic cold seep sediments and uncovered the potential mechanisms for involved microorganisms. High amounts of buried reactive Fe(III)/Mn(IV) minerals could be an important available electron acceptors for AOM. It is estimated that metal-AOM at least contributes 3% of total methane consumption from methanic sediments to the seep. Therefore, this research paper advances our understanding of the role of metal reduction to the global carbon cycle, especially the methane sink.

Evolutionary ecology of microbial populations inhabiting deep sea sediments associated with cold seeps.

Deep sea cold seep sediments host abundant and diverse microbial populations that significantly influence biogeochemical cycles. While numerous studies have revealed their community structure and functional capabilities, little is known about genetic heterogeneity within species. Here, we examine intraspecies diversity patterns of 39 abundant species identified in sediment layers down to 430 cm below the sea floor across six cold seep sites. These populations are grouped as aerobic methane-oxidizing bacteria, anaerobic methanotrophic archaea and sulfate-reducing bacteria. Different evolutionary trajectories are observed at the genomic level among these physiologically and phylogenetically diverse populations, with generally low rates of homologous recombination and strong purifying selection. Functional genes related to methane (pmoA and mcrA) and sulfate (dsrA) metabolisms are under strong purifying selection in most species investigated. These genes differ in evolutionary trajectories across phylogenetic clades but are functionally conserved across sites. Intrapopulation diversification of genomes and their mcrA and dsrA genes is depth-dependent and subject to different selection pressure throughout the sediment column redox zones at different sites. These results highlight the interplay between ecological processes and the evolution of key bacteria and archaea in deep sea cold seep extreme environments, shedding light on microbial adaptation in the subseafloor biosphere.

Metagenomic Views of Microbial Communities in Sand Sediments Associated with Coral Reefs.

Reef sediments, the home for microbes with high abundances, provide an important source of carbonates and nutrients for the growth and maintenance of coral reefs. However, there is a lack of systematic research on the composition of microbial community in sediments of different geographic sites and their potential effect on nutrient recycling and health of the coral reef ecosystem. In combination of biogeochemical measurements with gene- and genome-centric metagenomics, we assessed microbial community compositions and functional diversity, as well as profiles of antibiotic resistance genes in surface sediments of 16 coral reef sites at different depths from the Xisha islands in the South China Sea. Reef sediment microbiomes are diverse and novel at lower taxonomic ranks, dominated by Proteobacteria and Planctomycetota. Most reef sediment bacteria potentially participate in biogeochemical cycling via oxidizing various organic and inorganic compounds as energy sources. High abundances of Proteobacteria (mostly Rhizobiales and Woeseiales) are metabolically flexible and contain rhodopsin genes. Various classes of antibiotic resistance genes, hosted by diverse bacterial lineages, were identified to confer resistance to multidrug, aminoglycoside, and other antibiotics. Overall, our findings expanded the understanding of reef sediment microbial ecology and provided insights for their link to the coral reef ecosystem health.

A Novel Inovirus Reprograms Metabolism and Motility of Marine Alteromonas.

Members from the Inoviridae family with striking features are widespread, highly diverse, and ecologically pervasive across multiple hosts and environments. However, a small number of inoviruses have been isolated and studied. Here, a filamentous phage infecting Alteromonas abrolhosensis, designated ϕAFP1, was isolated from the South China Sea and represented a novel genus of Inoviridae. ϕAFP1 consisted of a single-stranded DNA genome (5986 bp), encoding eight putative ORFs. Comparative analyses revealed ϕAFP1 could be regarded as genetic mosaics having homologous sequences with Ralstonia and Stenotrophomonas phages. The temporal transcriptome analysis of A. abrolhosensis to ϕAFP1 infection revealed that 7.78% of the host genes were differentially expressed. The genes involved in translation processes, ribosome pathways, and degradation of multiple amino acid pathways at the plateau period were upregulated, while host material catabolic and bacterial motility-related genes were downregulated, indicating that ϕAFP1 might hijack the energy of the host for the synthesis of phage proteins. ϕAFP1 exerted step-by-step control on host genes through the appropriate level of utilizing host resources. Our study provided novel information for a better understanding of filamentous phage characteristics and phage-host interactions. IMPORTANCE Alteromonas is widely distributed and plays a vital role in biogeochemical in marine environments. However, little information about Alteromonas phages is available. Here, we isolated and characterized the biological characteristics and genome sequence of a novel inovirus infecting Alteromonas abrolhosensis, designated ϕAFP1, representing a novel viral genus of Inoviridae. We then presented a comprehensive view of the ϕAFP1 phage-Alteromonas abrolhosensis interactions, elucidating reprogramed host metabolism and motility. Our study provided novel information for better comprehension of filamentous phage characteristics and phage-host interactions.

Phylogenetically and catabolically diverse diazotrophs reside in deep-sea cold seep sediments.

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.

A mixed blessing of viruses in wastewater treatment plants.

Activated sludge of wastewater treatment plants harbors a very high diversity of both microorganisms and viruses, wherein the latter control microbial dynamics and metabolisms by infection and lysis of cells. However, it remains poorly understood how viruses impact the biochemical processes of activated sludge, for example in terms of treatment efficiency and pollutant removal. Using metagenomic and metatranscriptomic deep sequencing, the present study recovered thousands of viral sequences from activated sludge samples of three conventional wastewater treatment plants. Gene-sharing network indicated that most of viruses could not be assigned to known viral genera, implying activated sludge as an underexplored reservoir for new viruses and viral diversity. In silico predictions of virus-host linkages demonstrated that infected microbial hosts, mostly belonging to bacteria, were transcriptionally active and able to hydrolyze polymers including starches, celluloses, and proteins. Some viruses encode auxiliary metabolic genes (AMGs) involved in carbon, nitrogen, and sulfur cycling, and antibiotic resistance genes (ARGs) for resistance to multiple drugs. The virus-encoded AMGs may enhance the biodegradation of contaminants like starches and celluloses, suggesting a positive role for viruses in strengthening the performance of activated sludge. However, ARGs would be disseminated to different microorganisms using viruses as gene shuttles, demonstrating the possibility for viruses to facilitate the spread of antibiotic resistance in the environment. Collectively, this study highlights the mixed blessing of viruses in wastewater treatment plants, and deciphers how they manipulate the biochemical processes in the activated sludge, with implications for both environmental protection and ecosystem security.

Unveiling the occurrence, hosts and mobility potential of antibiotic resistance genes in the deep ocean.

As emerging microbial contaminants, antibiotic resistance genes (ARGs) are widely reported in the neritic zone. However, the profiles of ARGs in the deep ocean have not yet been fully resolved. In this study, the distribution, hosts, and mobility potential of ARGs at different water depths in the Western Pacific (WP) were investigated and compared to those in Bohai Sea (BH) waters using environmental parameter measurements, amplicon sequencing, metagenomic assembly and binning approaches. Our results showed that the top eight most abundant known ARG types in WP and BH waters were multidrug (39.85%), peptide (14.98%), aminoglycoside (11.33%), macrolide-lincosamide-streptogramin (MLS, 4.06%), tetracycline (3.74%), beta-lactam (3.12%), fluoroquinolone (1.79%) and rifamycin (1.24%). The ARGs observed in mesopelagic and bathypelagic waters were abundant and diverse as those observed in neritic waters, indicating that deep-sea water could be another environmental reservoir for ARGs. For deep-sea ARGs, members from classes Gammaproteobacteria (70%) and Alphaproteobacteria (21.1%) were the most important potential hosts. In addition, mobile genetic element analysis suggested that the ARG migration potential in dee sea water (> 1000 m) was relatively high. Overall, our findings expanded the understanding of ARGs in deep seawater and provided guidance for ARG pollution control and risk prediction.

Microbial ecology of sulfur cycling near the sulfate-methane transition of deep-sea cold seep sediments.

Microbial sulfate reduction is largely associated with anaerobic methane oxidation and alkane degradation in sulfate-methane transition zone (SMTZ) of deep-sea cold seeps. How the sulfur cycling is mediated by microbes near SMTZ has not been fully understood. In this study, we detected a shallow SMTZ in three of eight sediment cores sampled from two cold seep areas in the South China Sea. One hundred ten genomes representing sulfur-oxidizing bacteria (SOB) and sulfur-reducing bacteria (SRB) strains were identified from three SMTZ-bearing cores. In the layers above SMTZ, SOB were mostly constituted by Campylobacterota, Gammaproteobacteria and Alphaproteobacteria that probably depended on nitrogen oxides and/or oxygen for oxidation of sulfide and thiosulfate in near-surface sediment layers. In the layers below the SMTZ, the deltaproteobacterial SRB genomes and metatranscriptomes revealed CO2 fixation by Wood-Ljungdahl pathway, sulfate reduction and nitrogen fixation for syntrophic or fermentative lifestyle. A total of 68% of the metagenome assembled genomes were not adjacent to known species in a phylogenomic tree, indicating a high diversity of bacteria involved in sulfur cycling. With the large number of genomes for SOB and SRB, our study uncovers the microbial populations that potentially mediate sulfur metabolism and associated carbon and nitrogen cycles, which sheds light on complex biogeochemical processes in deep-sea environments.

Functional diversity of microbial communities in inactive seafloor sulfide deposits.

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.

Chemosynthetic and photosynthetic bacteria contribute differentially to primary production across a steep desert aridity gradient.

Desert soils harbour diverse communities of aerobic bacteria despite lacking substantial organic carbon inputs from vegetation. A major question is therefore how these communities maintain their biodiversity and biomass in these resource-limiting ecosystems. Here, we investigated desert topsoils and biological soil crusts collected along an aridity gradient traversing four climatic regions (sub-humid, semi-arid, arid, and hyper-arid). Metagenomic analysis indicated these communities vary in their capacity to use sunlight, organic compounds, and inorganic compounds as energy sources. Thermoleophilia, Actinobacteria, and Acidimicrobiia were the most abundant and prevalent bacterial classes across the aridity gradient in both topsoils and biocrusts. Contrary to the classical view that these taxa are obligate organoheterotrophs, genome-resolved analysis suggested they are metabolically flexible, with the capacity to also use atmospheric H2 to support aerobic respiration and often carbon fixation. In contrast, Cyanobacteria were patchily distributed and only abundant in certain biocrusts. Activity measurements profiled how aerobic H2 oxidation, chemosynthetic CO2 fixation, and photosynthesis varied with aridity. Cell-specific rates of atmospheric H2 consumption increased 143-fold along the aridity gradient, correlating with increased abundance of high-affinity hydrogenases. Photosynthetic and chemosynthetic primary production co-occurred throughout the gradient, with photosynthesis dominant in biocrusts and chemosynthesis dominant in arid and hyper-arid soils. Altogether, these findings suggest that the major bacterial lineages inhabiting hot deserts use different strategies for energy and carbon acquisition depending on resource availability. Moreover, they highlight the previously overlooked roles of Actinobacteriota as abundant primary producers and trace gases as critical energy sources supporting productivity and resilience of desert ecosystems.