Cargando…

Thermal acclimation of methanotrophs from the genus Methylobacter

Methanotrophs oxidize most of the methane (CH(4)) produced in natural and anthropogenic ecosystems. Often living close to soil surfaces, these microorganisms must frequently adjust to temperature change. While many environmental studies have addressed temperature effects on CH(4) oxidation and metha...

Descripción completa

Detalles Bibliográficos
Autores principales: Tveit, Alexander T., Söllinger, Andrea, Rainer, Edda Marie, Didriksen, Alena, Hestnes, Anne Grethe, Motleleng, Liabo, Hellinger, Hans-Jörg, Rattei, Thomas, Svenning, Mette M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10030640/
https://www.ncbi.nlm.nih.gov/pubmed/36650275
http://dx.doi.org/10.1038/s41396-023-01363-7
_version_ 1784910423102849024
author Tveit, Alexander T.
Söllinger, Andrea
Rainer, Edda Marie
Didriksen, Alena
Hestnes, Anne Grethe
Motleleng, Liabo
Hellinger, Hans-Jörg
Rattei, Thomas
Svenning, Mette M.
author_facet Tveit, Alexander T.
Söllinger, Andrea
Rainer, Edda Marie
Didriksen, Alena
Hestnes, Anne Grethe
Motleleng, Liabo
Hellinger, Hans-Jörg
Rattei, Thomas
Svenning, Mette M.
author_sort Tveit, Alexander T.
collection PubMed
description Methanotrophs oxidize most of the methane (CH(4)) produced in natural and anthropogenic ecosystems. Often living close to soil surfaces, these microorganisms must frequently adjust to temperature change. While many environmental studies have addressed temperature effects on CH(4) oxidation and methanotrophic communities, there is little knowledge about the physiological adjustments that underlie these effects. We have studied thermal acclimation in Methylobacter, a widespread, abundant, and environmentally important methanotrophic genus. Comparisons of growth and CH(4) oxidation kinetics at different temperatures in three members of the genus demonstrate that temperature has a strong influence on how much CH(4) is consumed to support growth at different CH(4) concentrations. However, the temperature effect varies considerably between species, suggesting that how a methanotrophic community is composed influences the temperature effect on CH(4) uptake. To understand thermal acclimation mechanisms widely we carried out a transcriptomics experiment with Methylobacter tundripaludum SV96(T). We observed, at different temperatures, how varying abundances of transcripts for glycogen and protein biosynthesis relate to cellular glycogen and ribosome concentrations. Our data also demonstrated transcriptional adjustment of CH(4) oxidation, oxidative phosphorylation, membrane fatty acid saturation, cell wall composition, and exopolysaccharides between temperatures. In addition, we observed differences in M. tundripaludum SV96(T) cell sizes at different temperatures. We conclude that thermal acclimation in Methylobacter results from transcriptional adjustment of central metabolism, protein biosynthesis, cell walls and storage. Acclimation leads to large shifts in CH(4) consumption and growth efficiency, but with major differences between species. Thus, our study demonstrates that physiological adjustments to temperature change can substantially influence environmental CH(4) uptake rates and that consideration of methanotroph physiology might be vital for accurate predictions of warming effects on CH(4) emissions.
format Online
Article
Text
id pubmed-10030640
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-100306402023-03-23 Thermal acclimation of methanotrophs from the genus Methylobacter Tveit, Alexander T. Söllinger, Andrea Rainer, Edda Marie Didriksen, Alena Hestnes, Anne Grethe Motleleng, Liabo Hellinger, Hans-Jörg Rattei, Thomas Svenning, Mette M. ISME J Article Methanotrophs oxidize most of the methane (CH(4)) produced in natural and anthropogenic ecosystems. Often living close to soil surfaces, these microorganisms must frequently adjust to temperature change. While many environmental studies have addressed temperature effects on CH(4) oxidation and methanotrophic communities, there is little knowledge about the physiological adjustments that underlie these effects. We have studied thermal acclimation in Methylobacter, a widespread, abundant, and environmentally important methanotrophic genus. Comparisons of growth and CH(4) oxidation kinetics at different temperatures in three members of the genus demonstrate that temperature has a strong influence on how much CH(4) is consumed to support growth at different CH(4) concentrations. However, the temperature effect varies considerably between species, suggesting that how a methanotrophic community is composed influences the temperature effect on CH(4) uptake. To understand thermal acclimation mechanisms widely we carried out a transcriptomics experiment with Methylobacter tundripaludum SV96(T). We observed, at different temperatures, how varying abundances of transcripts for glycogen and protein biosynthesis relate to cellular glycogen and ribosome concentrations. Our data also demonstrated transcriptional adjustment of CH(4) oxidation, oxidative phosphorylation, membrane fatty acid saturation, cell wall composition, and exopolysaccharides between temperatures. In addition, we observed differences in M. tundripaludum SV96(T) cell sizes at different temperatures. We conclude that thermal acclimation in Methylobacter results from transcriptional adjustment of central metabolism, protein biosynthesis, cell walls and storage. Acclimation leads to large shifts in CH(4) consumption and growth efficiency, but with major differences between species. Thus, our study demonstrates that physiological adjustments to temperature change can substantially influence environmental CH(4) uptake rates and that consideration of methanotroph physiology might be vital for accurate predictions of warming effects on CH(4) emissions. Nature Publishing Group UK 2023-01-18 2023-04 /pmc/articles/PMC10030640/ /pubmed/36650275 http://dx.doi.org/10.1038/s41396-023-01363-7 Text en © The Author(s) 2023 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Tveit, Alexander T.
Söllinger, Andrea
Rainer, Edda Marie
Didriksen, Alena
Hestnes, Anne Grethe
Motleleng, Liabo
Hellinger, Hans-Jörg
Rattei, Thomas
Svenning, Mette M.
Thermal acclimation of methanotrophs from the genus Methylobacter
title Thermal acclimation of methanotrophs from the genus Methylobacter
title_full Thermal acclimation of methanotrophs from the genus Methylobacter
title_fullStr Thermal acclimation of methanotrophs from the genus Methylobacter
title_full_unstemmed Thermal acclimation of methanotrophs from the genus Methylobacter
title_short Thermal acclimation of methanotrophs from the genus Methylobacter
title_sort thermal acclimation of methanotrophs from the genus methylobacter
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10030640/
https://www.ncbi.nlm.nih.gov/pubmed/36650275
http://dx.doi.org/10.1038/s41396-023-01363-7
work_keys_str_mv AT tveitalexandert thermalacclimationofmethanotrophsfromthegenusmethylobacter
AT sollingerandrea thermalacclimationofmethanotrophsfromthegenusmethylobacter
AT rainereddamarie thermalacclimationofmethanotrophsfromthegenusmethylobacter
AT didriksenalena thermalacclimationofmethanotrophsfromthegenusmethylobacter
AT hestnesannegrethe thermalacclimationofmethanotrophsfromthegenusmethylobacter
AT motlelengliabo thermalacclimationofmethanotrophsfromthegenusmethylobacter
AT hellingerhansjorg thermalacclimationofmethanotrophsfromthegenusmethylobacter
AT ratteithomas thermalacclimationofmethanotrophsfromthegenusmethylobacter
AT svenningmettem thermalacclimationofmethanotrophsfromthegenusmethylobacter