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A nitrite-oxidising bacterium constitutively consumes atmospheric hydrogen

Chemolithoautotrophic nitrite-oxidising bacteria (NOB) of the genus Nitrospira contribute to nitrification in diverse natural environments and engineered systems. Nitrospira are thought to be well-adapted to substrate limitation owing to their high affinity for nitrite and capacity to use alternativ...

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Autores principales: Leung, Pok Man, Daebeler, Anne, Chiri, Eleonora, Hanchapola, Iresha, Gillett, David L., Schittenhelm, Ralf B., Daims, Holger, Greening, Chris
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9381531/
https://www.ncbi.nlm.nih.gov/pubmed/35752717
http://dx.doi.org/10.1038/s41396-022-01265-0
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author Leung, Pok Man
Daebeler, Anne
Chiri, Eleonora
Hanchapola, Iresha
Gillett, David L.
Schittenhelm, Ralf B.
Daims, Holger
Greening, Chris
author_facet Leung, Pok Man
Daebeler, Anne
Chiri, Eleonora
Hanchapola, Iresha
Gillett, David L.
Schittenhelm, Ralf B.
Daims, Holger
Greening, Chris
author_sort Leung, Pok Man
collection PubMed
description Chemolithoautotrophic nitrite-oxidising bacteria (NOB) of the genus Nitrospira contribute to nitrification in diverse natural environments and engineered systems. Nitrospira are thought to be well-adapted to substrate limitation owing to their high affinity for nitrite and capacity to use alternative energy sources. Here, we demonstrate that the canonical nitrite oxidiser Nitrospira moscoviensis oxidises hydrogen (H(2)) below atmospheric levels using a high-affinity group 2a nickel-iron hydrogenase [K(m(app)) = 32 nM]. Atmospheric H(2) oxidation occurred under both nitrite-replete and nitrite-deplete conditions, suggesting low-potential electrons derived from H(2) oxidation promote nitrite-dependent growth and enable survival during nitrite limitation. Proteomic analyses confirmed the hydrogenase was abundant under both conditions and indicated extensive metabolic changes occur to reduce energy expenditure and growth under nitrite-deplete conditions. Thermodynamic modelling revealed that H(2) oxidation theoretically generates higher power yield than nitrite oxidation at low substrate concentrations and significantly contributes to growth at elevated nitrite concentrations. Collectively, this study suggests atmospheric H(2) oxidation enhances the growth and survival of NOB amid variability of nitrite supply, extends the phenomenon of atmospheric H(2) oxidation to an eighth phylum (Nitrospirota), and reveals unexpected new links between the global hydrogen and nitrogen cycles. Long classified as obligate nitrite oxidisers, our findings suggest H(2) may primarily support growth and survival of certain NOB in natural environments.
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spelling pubmed-93815312022-08-18 A nitrite-oxidising bacterium constitutively consumes atmospheric hydrogen Leung, Pok Man Daebeler, Anne Chiri, Eleonora Hanchapola, Iresha Gillett, David L. Schittenhelm, Ralf B. Daims, Holger Greening, Chris ISME J Article Chemolithoautotrophic nitrite-oxidising bacteria (NOB) of the genus Nitrospira contribute to nitrification in diverse natural environments and engineered systems. Nitrospira are thought to be well-adapted to substrate limitation owing to their high affinity for nitrite and capacity to use alternative energy sources. Here, we demonstrate that the canonical nitrite oxidiser Nitrospira moscoviensis oxidises hydrogen (H(2)) below atmospheric levels using a high-affinity group 2a nickel-iron hydrogenase [K(m(app)) = 32 nM]. Atmospheric H(2) oxidation occurred under both nitrite-replete and nitrite-deplete conditions, suggesting low-potential electrons derived from H(2) oxidation promote nitrite-dependent growth and enable survival during nitrite limitation. Proteomic analyses confirmed the hydrogenase was abundant under both conditions and indicated extensive metabolic changes occur to reduce energy expenditure and growth under nitrite-deplete conditions. Thermodynamic modelling revealed that H(2) oxidation theoretically generates higher power yield than nitrite oxidation at low substrate concentrations and significantly contributes to growth at elevated nitrite concentrations. Collectively, this study suggests atmospheric H(2) oxidation enhances the growth and survival of NOB amid variability of nitrite supply, extends the phenomenon of atmospheric H(2) oxidation to an eighth phylum (Nitrospirota), and reveals unexpected new links between the global hydrogen and nitrogen cycles. Long classified as obligate nitrite oxidisers, our findings suggest H(2) may primarily support growth and survival of certain NOB in natural environments. Nature Publishing Group UK 2022-06-25 2022-09 /pmc/articles/PMC9381531/ /pubmed/35752717 http://dx.doi.org/10.1038/s41396-022-01265-0 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/)
spellingShingle Article
Leung, Pok Man
Daebeler, Anne
Chiri, Eleonora
Hanchapola, Iresha
Gillett, David L.
Schittenhelm, Ralf B.
Daims, Holger
Greening, Chris
A nitrite-oxidising bacterium constitutively consumes atmospheric hydrogen
title A nitrite-oxidising bacterium constitutively consumes atmospheric hydrogen
title_full A nitrite-oxidising bacterium constitutively consumes atmospheric hydrogen
title_fullStr A nitrite-oxidising bacterium constitutively consumes atmospheric hydrogen
title_full_unstemmed A nitrite-oxidising bacterium constitutively consumes atmospheric hydrogen
title_short A nitrite-oxidising bacterium constitutively consumes atmospheric hydrogen
title_sort nitrite-oxidising bacterium constitutively consumes atmospheric hydrogen
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9381531/
https://www.ncbi.nlm.nih.gov/pubmed/35752717
http://dx.doi.org/10.1038/s41396-022-01265-0
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