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Aerobic H2 respiration enhances metabolic flexibility of methanotrophic bacteria

Carlo R. Carere, Kiel Hards, Karen M. Houghton, Jean F. Power, Ben McDonald, Christophe Collet, Daniel J. Gapes, Richard Sparling, Gregory M. Cook, Chris Greening, Matthew B. Stott
doi: https://doi.org/10.1101/075549
Carlo R. Carere
1Extremophile Research Group, GNS Science, Taupō, New Zealand.
2Scion, Te Papa Tipu Innovation Park, Private Bag 3020, Rotorua, New Zealand.
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Kiel Hards
3Department of Microbiology and Immunology, University of Otago, New Zealand.
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Karen M. Houghton
1Extremophile Research Group, GNS Science, Taupō, New Zealand.
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Jean F. Power
1Extremophile Research Group, GNS Science, Taupō, New Zealand.
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Ben McDonald
2Scion, Te Papa Tipu Innovation Park, Private Bag 3020, Rotorua, New Zealand.
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Christophe Collet
2Scion, Te Papa Tipu Innovation Park, Private Bag 3020, Rotorua, New Zealand.
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Daniel J. Gapes
2Scion, Te Papa Tipu Innovation Park, Private Bag 3020, Rotorua, New Zealand.
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Richard Sparling
4Department of Microbiology, University of Manitoba, Canada.
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Gregory M. Cook
3Department of Microbiology and Immunology, University of Otago, New Zealand.
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Chris Greening
3Department of Microbiology and Immunology, University of Otago, New Zealand.
5Land and Water Flagship, CSIRO, Australia.
6School of Biological Sciences, Monash University, Australia.
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  • For correspondence: chris.greening@monash.au m.stott@gns.cri.nz
Matthew B. Stott
1Extremophile Research Group, GNS Science, Taupō, New Zealand.
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  • For correspondence: chris.greening@monash.au m.stott@gns.cri.nz
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Abstract

Methanotrophic bacteria are important soil biofilters for the climate-active gas methane. The prevailing opinion is that these bacteria exclusively metabolise single-carbon, and in limited instances, short-chain hydrocarbons for growth. This specialist lifestyle juxtaposes metabolic flexibility, a key strategy for environmental adaptation of microorganisms. Here we show that a methanotrophic bacterium from the phylum Verrucomicrobia oxidises hydrogen gas (H2) during growth and persistence. Methylacidiphilum sp. RTK17.1 expresses a membrane-bound hydrogenase to aerobically respire molecular H2 at environmentally significant concentrations. While H2 oxidation did not support growth as the sole electron source, it significantly enhanced mixotrophic growth yields under both oxygen-replete and oxygen-limiting conditions and was sustained in non-growing cultures starved for methane. We propose that H2 is consumed by this bacterium for mixotrophic growth and persistence in a manner similar to other non-methanotrophic soil microorganisms. We have identified genes encoding oxygen-tolerant uptake hydrogenases in all publicly-available methanotroph genomes, suggesting that H2 oxidation serves a general strategy for methanotrophs to remain energised in chemically-limited environments.

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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 September 16, 2016.
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Aerobic H2 respiration enhances metabolic flexibility of methanotrophic bacteria
Carlo R. Carere, Kiel Hards, Karen M. Houghton, Jean F. Power, Ben McDonald, Christophe Collet, Daniel J. Gapes, Richard Sparling, Gregory M. Cook, Chris Greening, Matthew B. Stott
bioRxiv 075549; doi: https://doi.org/10.1101/075549
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Aerobic H2 respiration enhances metabolic flexibility of methanotrophic bacteria
Carlo R. Carere, Kiel Hards, Karen M. Houghton, Jean F. Power, Ben McDonald, Christophe Collet, Daniel J. Gapes, Richard Sparling, Gregory M. Cook, Chris Greening, Matthew B. Stott
bioRxiv 075549; doi: https://doi.org/10.1101/075549

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