Summary
Gas hydrates harbor 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, metal (iron/manganese) reduction zone, and 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 (TRAP) 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.
Originality-Significance Statement This work provides insights into the metabolism and adaptations of microbes that are ubiquitous and abundant in methane-rich ecosystems. Our findings suggest that bacterial fermentation is a source of acetate for aceticlastic methanogenesis and a driver of iron reduction in the metal reduction zone. Atribacteria, the most abundant phylum in gas hydrate-bearing sediments, possess multiple strategies to cope with environmental stress.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
↵# Now at: Michigan Medicine, University of Michigan, Ann Arbor, Michigan, USA
↵§ Now at: Association of Public Health Laboratories, Manager of Emerging and Zoonotic Infectious Diseases, Silver Spring, MD, USA
Dedication: To Katrina Edwards
We made numerous changes to update the text and based on reviewer suggestions. We updated the text and tables of top protein BLAST hits to reflect the latest database searches as of June 2021 and updated the manuscript to cover the results of key Atribacteria studies published since 2019 including Liu et al 2019 ISME J, Bird et al 2019 mBio, Katayama et al 2019 and Chakraborty et al. 2020. We also remade Figures 1-4 based on reviewer comments and new findings since the original submission.
