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Sulfur and methane oxidation by a single microorganism

Natural and anthropogenic wetlands are major sources of the atmospheric greenhouse gas methane. Methane emissions from wetlands are mitigated by methanotrophic bacteria at the oxic–anoxic interface, a zone of intense redox cycling of carbon, sulfur, and nitrogen compounds. Here, we report on the iso...

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Autores principales: Gwak, Joo-Han, Awala, Samuel Imisi, Nguyen, Ngoc-Loi, Yu, Woon-Jong, Yang, Hae-Young, von Bergen, Martin, Jehmlich, Nico, Kits, K. Dimitri, Loy, Alexander, Dunfield, Peter. F., Dahl, Christiane, Hyun, Jung-Ho, Rhee, Sung-Keun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9371685/
https://www.ncbi.nlm.nih.gov/pubmed/35914169
http://dx.doi.org/10.1073/pnas.2114799119
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author Gwak, Joo-Han
Awala, Samuel Imisi
Nguyen, Ngoc-Loi
Yu, Woon-Jong
Yang, Hae-Young
von Bergen, Martin
Jehmlich, Nico
Kits, K. Dimitri
Loy, Alexander
Dunfield, Peter. F.
Dahl, Christiane
Hyun, Jung-Ho
Rhee, Sung-Keun
author_facet Gwak, Joo-Han
Awala, Samuel Imisi
Nguyen, Ngoc-Loi
Yu, Woon-Jong
Yang, Hae-Young
von Bergen, Martin
Jehmlich, Nico
Kits, K. Dimitri
Loy, Alexander
Dunfield, Peter. F.
Dahl, Christiane
Hyun, Jung-Ho
Rhee, Sung-Keun
author_sort Gwak, Joo-Han
collection PubMed
description Natural and anthropogenic wetlands are major sources of the atmospheric greenhouse gas methane. Methane emissions from wetlands are mitigated by methanotrophic bacteria at the oxic–anoxic interface, a zone of intense redox cycling of carbon, sulfur, and nitrogen compounds. Here, we report on the isolation of an aerobic methanotrophic bacterium, ‘Methylovirgula thiovorans' strain HY1, which possesses metabolic capabilities never before found in any methanotroph. Most notably, strain HY1 is the first bacterium shown to aerobically oxidize both methane and reduced sulfur compounds for growth. Genomic and proteomic analyses showed that soluble methane monooxygenase and XoxF-type alcohol dehydrogenases are responsible for methane and methanol oxidation, respectively. Various pathways for respiratory sulfur oxidation were present, including the Sox–rDsr pathway and the S(4)I system. Strain HY1 employed the Calvin–Benson–Bassham cycle for CO(2) fixation during chemolithoautotrophic growth on reduced sulfur compounds. Proteomic and microrespirometry analyses showed that the metabolic pathways for methane and thiosulfate oxidation were induced in the presence of the respective substrates. Methane and thiosulfate could therefore be independently or simultaneously oxidized. The discovery of this versatile bacterium demonstrates that methanotrophy and thiotrophy are compatible in a single microorganism and underpins the intimate interactions of methane and sulfur cycles in oxic–anoxic interface environments.
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spelling pubmed-93716852022-08-12 Sulfur and methane oxidation by a single microorganism Gwak, Joo-Han Awala, Samuel Imisi Nguyen, Ngoc-Loi Yu, Woon-Jong Yang, Hae-Young von Bergen, Martin Jehmlich, Nico Kits, K. Dimitri Loy, Alexander Dunfield, Peter. F. Dahl, Christiane Hyun, Jung-Ho Rhee, Sung-Keun Proc Natl Acad Sci U S A Biological Sciences Natural and anthropogenic wetlands are major sources of the atmospheric greenhouse gas methane. Methane emissions from wetlands are mitigated by methanotrophic bacteria at the oxic–anoxic interface, a zone of intense redox cycling of carbon, sulfur, and nitrogen compounds. Here, we report on the isolation of an aerobic methanotrophic bacterium, ‘Methylovirgula thiovorans' strain HY1, which possesses metabolic capabilities never before found in any methanotroph. Most notably, strain HY1 is the first bacterium shown to aerobically oxidize both methane and reduced sulfur compounds for growth. Genomic and proteomic analyses showed that soluble methane monooxygenase and XoxF-type alcohol dehydrogenases are responsible for methane and methanol oxidation, respectively. Various pathways for respiratory sulfur oxidation were present, including the Sox–rDsr pathway and the S(4)I system. Strain HY1 employed the Calvin–Benson–Bassham cycle for CO(2) fixation during chemolithoautotrophic growth on reduced sulfur compounds. Proteomic and microrespirometry analyses showed that the metabolic pathways for methane and thiosulfate oxidation were induced in the presence of the respective substrates. Methane and thiosulfate could therefore be independently or simultaneously oxidized. The discovery of this versatile bacterium demonstrates that methanotrophy and thiotrophy are compatible in a single microorganism and underpins the intimate interactions of methane and sulfur cycles in oxic–anoxic interface environments. National Academy of Sciences 2022-08-01 2022-08-09 /pmc/articles/PMC9371685/ /pubmed/35914169 http://dx.doi.org/10.1073/pnas.2114799119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Gwak, Joo-Han
Awala, Samuel Imisi
Nguyen, Ngoc-Loi
Yu, Woon-Jong
Yang, Hae-Young
von Bergen, Martin
Jehmlich, Nico
Kits, K. Dimitri
Loy, Alexander
Dunfield, Peter. F.
Dahl, Christiane
Hyun, Jung-Ho
Rhee, Sung-Keun
Sulfur and methane oxidation by a single microorganism
title Sulfur and methane oxidation by a single microorganism
title_full Sulfur and methane oxidation by a single microorganism
title_fullStr Sulfur and methane oxidation by a single microorganism
title_full_unstemmed Sulfur and methane oxidation by a single microorganism
title_short Sulfur and methane oxidation by a single microorganism
title_sort sulfur and methane oxidation by a single microorganism
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9371685/
https://www.ncbi.nlm.nih.gov/pubmed/35914169
http://dx.doi.org/10.1073/pnas.2114799119
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