Genomic Reconstruction of an Uncultured Hydrothermal Vent Gammaproteobacterial Methanotroph (Family Methylothermaceae) Indicates Multiple Adaptations to Oxygen Limitation

Creators: Skennerton, Connor T.; Ward, Lewis M.; Michel, Alice; Metcalfe, Kyle; Valiente, Chanel; Mullin, Sean; Chan, Ken Y.; Gradinaru, Viviana; Orphan, Victoria J.

Abstract

Hydrothermal vents are an important contributor to marine biogeochemistry, producing large volumes of reduced fluids, gasses, and metals and housing unique, productive microbial and animal communities fueled by chemosynthesis. Methane is a common constituent of hydrothermal vent fluid and is frequently consumed at vent sites by methanotrophic bacteria that serve to control escape of this greenhouse gas into the atmosphere. Despite their ecological and geochemical importance, little is known about the ecophysiology of uncultured hydrothermal vent-associated methanotrophic bacteria. Using metagenomic binning techniques, we recovered and analyzed a near-complete genome from a novel gammaproteobacterial methanotroph (B42) associated with a white smoker chimney in the Southern Lau basin. B42 was the dominant methanotroph in the community, at ∼80x coverage, with only four others detected in the metagenome, all on low coverage contigs (7x–12x). Phylogenetic placement of B42 showed it is a member of the Methylothermaceae, a family currently represented by only one sequenced genome. Metabolic inferences based on the presence of known pathways in the genome showed that B42 possesses a branched respiratory chain with A- and B-family heme copper oxidases, cytochrome bd oxidase and a partial denitrification pathway. These genes could allow B42 to respire over a wide range of oxygen concentrations within the highly dynamic vent environment. Phylogenies of the denitrification genes revealed they are the result of separate horizontal gene transfer from other Proteobacteria and suggest that denitrification is a selective advantage in conditions where extremely low oxygen concentrations require all oxygen to be used for methane activation.

Additional Information

© 2015 Skennerton, Ward, Michel, Metcalfe, Valiente, Mullin, Chan, Gradinaru and Orphan. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. Received: 02 October 2015; Accepted: 30 November 2015; Published: 23 December 2015. The metagenomic analysis and annotation for B42 was done in part by the students of the GeBI 246 Molecular Geobiology course at Caltech. We thank Ben Harrison for XRD analysis on sample #2044C and Patty Tavormina for assistance during the course and critical reading of this manuscript. We also thank Chief Scientist Robert Vrijenhoek (Monterey Bay Aquarium Research Institute) for providing the opportunity to collect samples during the 2005 tuim06mv cruise. We thank Igor Antoshechkin of the Millard and Muriel Jacobs Genetics and Genomics Laboratory at Caltech for his services and input during sequencing of the genomic library. This research was supported in part by a grant from the NASA Astrobiology Institute (Award # NNA13AA92A) and the Gordon and Betty Moore Foundation Marine Microbiology Initiative (GBMF3780) to VO. This is NAI-Life Underground Publication Number 070. Part of this work was supported by grants to VG: NIH 1R21MH103824-01; the Gordon and Betty Moore Foundation through Grant GBMF2809 to the Caltech Programmable Molecular Technology Initiative and by the Beckman Institute for Optogenetics and CLARITY. KC is supported by the NIH Predoctoral Training in Biology and Chemistry grant (2T32GM007616-36). LW was supported by an NSF Graduate Research Fellowship. Sample collection from the Tu'i Malila vent field was funded by the National Science Foundation (NSF), grant number NSF OCE-0241613, awarded to Robert Vrijenhoek. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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