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Hydrogen Oxidation Influences Glycogen Accumulation in a Verrucomicrobial Methanotroph
Metabolic flexibility in aerobic methane oxidizing bacteria (methanotrophs) enhances cell growth and survival in instances where resources are variable or limiting. Examples include the production of intracellular compounds (such as glycogen or polyhydroxyalkanoates) in response to unbalanced growth...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2019
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6706786/ https://www.ncbi.nlm.nih.gov/pubmed/31474959 http://dx.doi.org/10.3389/fmicb.2019.01873 |
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author | Carere, Carlo R. McDonald, Ben Peach, Hanna A. Greening, Chris Gapes, Daniel J. Collet, Christophe Stott, Matthew B. |
author_facet | Carere, Carlo R. McDonald, Ben Peach, Hanna A. Greening, Chris Gapes, Daniel J. Collet, Christophe Stott, Matthew B. |
author_sort | Carere, Carlo R. |
collection | PubMed |
description | Metabolic flexibility in aerobic methane oxidizing bacteria (methanotrophs) enhances cell growth and survival in instances where resources are variable or limiting. Examples include the production of intracellular compounds (such as glycogen or polyhydroxyalkanoates) in response to unbalanced growth conditions and the use of some energy substrates, besides methane, when available. Indeed, recent studies show that verrucomicrobial methanotrophs can grow mixotrophically through oxidation of hydrogen and methane gases via respiratory membrane-bound group 1d [NiFe] hydrogenases and methane monooxygenases, respectively. Hydrogen metabolism is particularly important for adaptation to methane and oxygen limitation, suggesting this metabolic flexibility may confer growth and survival advantages. In this work, we provide evidence that, in adopting a mixotrophic growth strategy, the thermoacidophilic methanotroph, Methylacidiphilum sp. RTK17.1 changes its growth rate, biomass yields and the production of intracellular glycogen reservoirs. Under nitrogen-fixing conditions, removal of hydrogen from the feed-gas resulted in a 14% reduction in observed growth rates and a 144% increase in cellular glycogen content. Concomitant with increases in glycogen content, the total protein content of biomass decreased following the removal of hydrogen. Transcriptome analysis of Methylacidiphilum sp. RTK17.1 revealed a 3.5-fold upregulation of the Group 1d [NiFe] hydrogenase in response to oxygen limitation and a 4-fold upregulation of nitrogenase encoding genes (nifHDKENX) in response to nitrogen limitation. Genes associated with glycogen synthesis and degradation were expressed constitutively and did not display evidence of transcriptional regulation. Collectively these data further challenge the belief that hydrogen metabolism in methanotrophic bacteria is primarily associated with energy conservation during nitrogen fixation and suggests its utilization provides a competitive growth advantage within hypoxic habitats. |
format | Online Article Text |
id | pubmed-6706786 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-67067862019-08-30 Hydrogen Oxidation Influences Glycogen Accumulation in a Verrucomicrobial Methanotroph Carere, Carlo R. McDonald, Ben Peach, Hanna A. Greening, Chris Gapes, Daniel J. Collet, Christophe Stott, Matthew B. Front Microbiol Microbiology Metabolic flexibility in aerobic methane oxidizing bacteria (methanotrophs) enhances cell growth and survival in instances where resources are variable or limiting. Examples include the production of intracellular compounds (such as glycogen or polyhydroxyalkanoates) in response to unbalanced growth conditions and the use of some energy substrates, besides methane, when available. Indeed, recent studies show that verrucomicrobial methanotrophs can grow mixotrophically through oxidation of hydrogen and methane gases via respiratory membrane-bound group 1d [NiFe] hydrogenases and methane monooxygenases, respectively. Hydrogen metabolism is particularly important for adaptation to methane and oxygen limitation, suggesting this metabolic flexibility may confer growth and survival advantages. In this work, we provide evidence that, in adopting a mixotrophic growth strategy, the thermoacidophilic methanotroph, Methylacidiphilum sp. RTK17.1 changes its growth rate, biomass yields and the production of intracellular glycogen reservoirs. Under nitrogen-fixing conditions, removal of hydrogen from the feed-gas resulted in a 14% reduction in observed growth rates and a 144% increase in cellular glycogen content. Concomitant with increases in glycogen content, the total protein content of biomass decreased following the removal of hydrogen. Transcriptome analysis of Methylacidiphilum sp. RTK17.1 revealed a 3.5-fold upregulation of the Group 1d [NiFe] hydrogenase in response to oxygen limitation and a 4-fold upregulation of nitrogenase encoding genes (nifHDKENX) in response to nitrogen limitation. Genes associated with glycogen synthesis and degradation were expressed constitutively and did not display evidence of transcriptional regulation. Collectively these data further challenge the belief that hydrogen metabolism in methanotrophic bacteria is primarily associated with energy conservation during nitrogen fixation and suggests its utilization provides a competitive growth advantage within hypoxic habitats. Frontiers Media S.A. 2019-08-16 /pmc/articles/PMC6706786/ /pubmed/31474959 http://dx.doi.org/10.3389/fmicb.2019.01873 Text en Copyright © 2019 Carere, McDonald, Peach, Greening, Gapes, Collet and Stott. http://creativecommons.org/licenses/by/4.0/ 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) and the copyright owner(s) 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. |
spellingShingle | Microbiology Carere, Carlo R. McDonald, Ben Peach, Hanna A. Greening, Chris Gapes, Daniel J. Collet, Christophe Stott, Matthew B. Hydrogen Oxidation Influences Glycogen Accumulation in a Verrucomicrobial Methanotroph |
title | Hydrogen Oxidation Influences Glycogen Accumulation in a Verrucomicrobial Methanotroph |
title_full | Hydrogen Oxidation Influences Glycogen Accumulation in a Verrucomicrobial Methanotroph |
title_fullStr | Hydrogen Oxidation Influences Glycogen Accumulation in a Verrucomicrobial Methanotroph |
title_full_unstemmed | Hydrogen Oxidation Influences Glycogen Accumulation in a Verrucomicrobial Methanotroph |
title_short | Hydrogen Oxidation Influences Glycogen Accumulation in a Verrucomicrobial Methanotroph |
title_sort | hydrogen oxidation influences glycogen accumulation in a verrucomicrobial methanotroph |
topic | Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6706786/ https://www.ncbi.nlm.nih.gov/pubmed/31474959 http://dx.doi.org/10.3389/fmicb.2019.01873 |
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