Microbial metabolism and adaptations in Atribacteria‐dominated methane hydrate sediments

Abstract

Summary Gas hydrates harbour gigatons of natural gas, yet their microbiomes remain understudied. We bioprospected 16S rRNA amplicons, metagenomes, and metaproteomes from methane hydrate‐bearing sediments under Hydrate Ridge (offshore Oregon, USA, ODP Site 1244, 2–69 mbsf) for novel microbial metabolic and biosynthetic potential. Atribacteria sequences generally increased in relative sequence abundance with increasing sediment depth. Most Atribacteria ASVs belonged to JS‐1‐Genus 1 and clustered with other sequences from gas hydrate‐bearing sediments. We recovered 21 metagenome‐assembled genomic bins spanning three geochemical zones in the sediment core: the sulfate–methane transition zone, the metal (iron/manganese) reduction zone, and the gas hydrate stability zone. We found evidence for bacterial fermentation as a source of acetate for aceticlastic methanogenesis and as a driver of iron reduction in the metal reduction zone. In multiple zones, we identified a Ni‐Fe hydrogenase‐Na+/H+ antiporter supercomplex (Hun) in Atribacteria and Firmicutes bins and in other deep subsurface bacteria and cultured hyperthermophiles from the Thermotogae phylum. Atribacteria expressed tripartite ATP‐independent transporters downstream from a novel regulator (AtiR). Atribacteria also possessed adaptations to survive extreme conditions (e.g. high salt brines, high pressure and cold temperatures) including the ability to synthesize the osmolyte di‐myo‐inositol‐phosphate as well as expression of K+‐stimulated pyrophosphatase and capsule proteins.

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

“…While members of the Caldatribacteriota phylum are prevalent in cold seep sediments 11 , 40 , no previous studies have inferred that they are diazotrophic. These results highlight that Caldatribacteriota may play biogeochemically and ecologically significant roles within diverse cold seeps besides their role in carbon cycling 66 . Most other diazotrophs are at lower abundance (<1% of the microbial community).…”

“…The study would not have been possible without publicly available genomic data from already published studies, and the authors wish to acknowledge all the participants, organizations, and funding agencies that contributed to the collection and analysis of all the data utilized in our study, including those acknowledged in refs. 66 , 82 – 85 . Detailed references are listed in Supplementary Data 1 .…”

METABOLIC: high-throughput profiling of microbial genomes for functional traits, metabolism, biogeochemistry, and community-scale functional networks

“…To benchmark and test the performance of METABOLIC in different environments, eight datasets of metagenomes and metagenomic reads from marine, terrestrial, and human environments were used. These included marine subsurface sediments [ 55 ] (Deep biosphere beneath Hydrate Ridge offshore Oregon), freshwater lake [ 56 ] (Lake Tanganyika, eastern Africa), colorectal cancer (CRC) patient gut [ 57 ], healthy human gut [ 57 ], deep-sea hydrothermal vent [ 53 ] (Guaymas Basin, Gulf of California), terrestrial subsurface sediments and water [ 2 ] (Rifle, CO, USA), meadow soils [ 58 ] (Angelo Coastal Range Reserve, CA, USA), and advanced water treatment facility [ 59 ] (Groundwater Replenishment System, Orange County, CA, USA). Default settings were used for running METABOLIC-C.…”

“…To compare the metabolic profile of two environments at the community scale, MW-score was used as the benchmark. Two sets of environmental pairs were compared, including the pair of marine subsurface sediments [ 55 ] and terrestrial subsurface sediments [ 2 ] and the pair of freshwater lake [ 56 ] and deep-sea hydrothermal vent [ 53 ]. To demonstrate differences between these environments in specific biogeochemical processes, we focused on the biogeochemical cycling of sulfur.…”

The Inositol Phosphate System—A Coordinator of Metabolic Adaptability

“…This interconnectedness is dramatically illustrated under conditions of total inositol depletion, which results in the “inositol-less” death of cultured cells within hours [ 3 ]. Importantly, many key components and metabolic functions of the inositol system are conserved across eukaryotes, indicating that these molecules influence metabolism and energy homeostasis across the evolutionary timeline [ 4 , 5 , 6 ]. In this review, we examine the influence of the inositol phosphate system on the coordination of nutrient sensing and bioenergetic pathways to highlight its many roles in metabolic function and argue that this system should be viewed as a single network with respect to nutrient metabolism and bioenergetic homeostasis.…”