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Adaptations of Atribacteria to life in methane hydrates: hot traits for cold life

View ORCID ProfileJennifer B. Glass, Piyush Ranjan, View ORCID ProfileCecilia B. Kretz, View ORCID ProfileBrook L. Nunn, Abigail M. Johnson, James McManus, View ORCID ProfileFrank J. Stewart
doi: https://doi.org/10.1101/536078
Jennifer B. Glass
1School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA, USA
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  • For correspondence: jennifer.glass@eas.gatech.edu
Piyush Ranjan
2School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, USA
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Cecilia B. Kretz
1School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA, USA
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  • ORCID record for Cecilia B. Kretz
Brook L. Nunn
3Department of Genome Sciences, University of Washington, Seattle, WA
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Abigail M. Johnson
1School of Earth and Atmospheric Sciences, Georgia Institute of Technology, Atlanta, GA, USA
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James McManus
4Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, USA
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Frank J. Stewart
2School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, USA
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Summary

Gas hydrates harbor gigatons of natural gas, yet their microbiomes remain mysterious. We bioprospected methane hydrate-bearing sediments from under Hydrate Ridge (offshore Oregon, USA, ODP Site 1244) using 16S rRNA gene amplicon, metagenomic, and metaproteomic analysis. Atribacteria (JS-1 Genus 1) sequences rose in abundance with increasing sediment depth. We characterized the most complete JS-1 Genus 1 metagenome-assembled genomic bin (B2) from the deepest sample, 69 meters below the seafloor (E10-H5), within the gas hydrate stability zone. B2 harbors functions not previously reported for Atribacteria, including a primitive respiratory complex and myriad capabilities to survive extreme conditions (e.g. high salt brines, high pressure, and cold temperatures). Several Atribacteria traits, such as a hydrogenase-Na+/H+ antiporter supercomplex (Hun) and di-myo-inositol-phosphate (DIP) synthesis, were similar to those from hyperthermophilic archaea. Expressed Atribacteria proteins were involved in transport of branched chain amino acids and carboxylic acids. Transporter genes were downstream from a novel helix-turn-helix transcriptional regulator, AtiR, which was not present in Atribacteria from other sites. Overall, Atribacteria appear to be endowed with unique strategies that may contribute to its dominance in methane-hydrate bearing sediments. Active microbial transport of amino and carboxylic acids in the gas hydrate stability zone may influence gas hydrate stability.

Originality-Significance Statement This work provides insights into the metabolism and adaptations of elusive Atribacteria (JS-1 clade) that are ubiquitous and abundant in methane-rich ecosystems. We show that JS-1 (Genus 1) from methane hydrate stability zones contain metabolisms and stress survival strategies similar to hyperthermophilic archaea.

Footnotes

  • ↵# Now at: Michigan Medicine, University of Michigan, Ann Arbor, Michigan, USA;

  • ↵§ Now at: Division of Scientific Education and Professional Development, Epidemiology Workforce Branch, Laboratory Leadership Service, Field Assignee New York City Public Health Laboratory, Centers for Disease Control and Prevention, Atlanta, Georgia, USA

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 31, 2019.
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Adaptations of Atribacteria to life in methane hydrates: hot traits for cold life
Jennifer B. Glass, Piyush Ranjan, Cecilia B. Kretz, Brook L. Nunn, Abigail M. Johnson, James McManus, Frank J. Stewart
bioRxiv 536078; doi: https://doi.org/10.1101/536078
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Adaptations of Atribacteria to life in methane hydrates: hot traits for cold life
Jennifer B. Glass, Piyush Ranjan, Cecilia B. Kretz, Brook L. Nunn, Abigail M. Johnson, James McManus, Frank J. Stewart
bioRxiv 536078; doi: https://doi.org/10.1101/536078

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