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More Than a Methanotroph: A Broader Substrate Spectrum for Methylacidiphilum fumariolicum SolV

Volcanic areas emit a number of gases including methane and other short chain alkanes, that may serve as energy source for the prevailing microorganisms. The verrucomicrobial methanotroph Methylacidiphilum fumariolicum SolV was isolated from a volcanic mud pot, and is able to grow under thermoacidop...

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Autores principales: Picone, Nunzia, Mohammadi, Sepehr S., Waajen, Annemiek C., van Alen, Theo A., Jetten, Mike S. M., Pol, Arjan, Op den Camp, Huub J. M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7768010/
https://www.ncbi.nlm.nih.gov/pubmed/33381099
http://dx.doi.org/10.3389/fmicb.2020.604485
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author Picone, Nunzia
Mohammadi, Sepehr S.
Waajen, Annemiek C.
van Alen, Theo A.
Jetten, Mike S. M.
Pol, Arjan
Op den Camp, Huub J. M.
author_facet Picone, Nunzia
Mohammadi, Sepehr S.
Waajen, Annemiek C.
van Alen, Theo A.
Jetten, Mike S. M.
Pol, Arjan
Op den Camp, Huub J. M.
author_sort Picone, Nunzia
collection PubMed
description Volcanic areas emit a number of gases including methane and other short chain alkanes, that may serve as energy source for the prevailing microorganisms. The verrucomicrobial methanotroph Methylacidiphilum fumariolicum SolV was isolated from a volcanic mud pot, and is able to grow under thermoacidophilic conditions on different gaseous substrates. Its genome contains three operons encoding a particulate methane monooxygenase (pMMO), the enzyme that converts methane to methanol. The expression of two of these pmo operons is subjected to oxygen-dependent regulation, whereas the expression of the third copy (pmoCAB3) has, so far, never been reported. In this study we investigated the ability of strain SolV to utilize short-chain alkanes and monitored the expression of the pmo operons under different conditions. In batch cultures and in carbon-limited continuous cultures, strain SolV was able to oxidize and grow on C(1)–C(3) compounds. Oxidation of ethane did occur simultaneously with methane, while propane consumption only started once methane and ethane became limited. Butane oxidation was not observed. Transcriptome data showed that pmoCAB1 and pmoCAB3 were induced in the absence of methane and the expression of pmoCAB3 increased upon propane addition. Together the results of our study unprecedently show that a pMMO-containing methanotroph is able to co-metabolize other gaseous hydrocarbons, beside methane. Moreover, it expands the substrate spectrum of verrucomicrobial methanotrophs, supporting their high metabolic flexibility and adaptation to the harsh and dynamic conditions in volcanic ecosystems.
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spelling pubmed-77680102020-12-29 More Than a Methanotroph: A Broader Substrate Spectrum for Methylacidiphilum fumariolicum SolV Picone, Nunzia Mohammadi, Sepehr S. Waajen, Annemiek C. van Alen, Theo A. Jetten, Mike S. M. Pol, Arjan Op den Camp, Huub J. M. Front Microbiol Microbiology Volcanic areas emit a number of gases including methane and other short chain alkanes, that may serve as energy source for the prevailing microorganisms. The verrucomicrobial methanotroph Methylacidiphilum fumariolicum SolV was isolated from a volcanic mud pot, and is able to grow under thermoacidophilic conditions on different gaseous substrates. Its genome contains three operons encoding a particulate methane monooxygenase (pMMO), the enzyme that converts methane to methanol. The expression of two of these pmo operons is subjected to oxygen-dependent regulation, whereas the expression of the third copy (pmoCAB3) has, so far, never been reported. In this study we investigated the ability of strain SolV to utilize short-chain alkanes and monitored the expression of the pmo operons under different conditions. In batch cultures and in carbon-limited continuous cultures, strain SolV was able to oxidize and grow on C(1)–C(3) compounds. Oxidation of ethane did occur simultaneously with methane, while propane consumption only started once methane and ethane became limited. Butane oxidation was not observed. Transcriptome data showed that pmoCAB1 and pmoCAB3 were induced in the absence of methane and the expression of pmoCAB3 increased upon propane addition. Together the results of our study unprecedently show that a pMMO-containing methanotroph is able to co-metabolize other gaseous hydrocarbons, beside methane. Moreover, it expands the substrate spectrum of verrucomicrobial methanotrophs, supporting their high metabolic flexibility and adaptation to the harsh and dynamic conditions in volcanic ecosystems. Frontiers Media S.A. 2020-12-14 /pmc/articles/PMC7768010/ /pubmed/33381099 http://dx.doi.org/10.3389/fmicb.2020.604485 Text en Copyright © 2020 Picone, Mohammadi, Waajen, van Alen, Jetten, Pol and Op den Camp. 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
Picone, Nunzia
Mohammadi, Sepehr S.
Waajen, Annemiek C.
van Alen, Theo A.
Jetten, Mike S. M.
Pol, Arjan
Op den Camp, Huub J. M.
More Than a Methanotroph: A Broader Substrate Spectrum for Methylacidiphilum fumariolicum SolV
title More Than a Methanotroph: A Broader Substrate Spectrum for Methylacidiphilum fumariolicum SolV
title_full More Than a Methanotroph: A Broader Substrate Spectrum for Methylacidiphilum fumariolicum SolV
title_fullStr More Than a Methanotroph: A Broader Substrate Spectrum for Methylacidiphilum fumariolicum SolV
title_full_unstemmed More Than a Methanotroph: A Broader Substrate Spectrum for Methylacidiphilum fumariolicum SolV
title_short More Than a Methanotroph: A Broader Substrate Spectrum for Methylacidiphilum fumariolicum SolV
title_sort more than a methanotroph: a broader substrate spectrum for methylacidiphilum fumariolicum solv
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7768010/
https://www.ncbi.nlm.nih.gov/pubmed/33381099
http://dx.doi.org/10.3389/fmicb.2020.604485
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