Methanotroph-methylotroph lipid adaptations to changing environmental conditions

Methanotrophs, in particular methane-oxidizing bacteria (MOB), regulate the release of methane from lakes, and often co-occur with methylotrophs that may enhance methane-oxidation rates. Assessing the interaction and physiological status of these two microbial groups is essential for determining the...

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Main Authors: Nora Richter, Laura Villanueva, Ellen C. Hopmans, Nicole J. Bale, Jaap S. Sinninghe Damsté, Darci Rush
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-02-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2025.1532719/full
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author Nora Richter
Laura Villanueva
Laura Villanueva
Ellen C. Hopmans
Nicole J. Bale
Jaap S. Sinninghe Damsté
Jaap S. Sinninghe Damsté
Darci Rush
author_facet Nora Richter
Laura Villanueva
Laura Villanueva
Ellen C. Hopmans
Nicole J. Bale
Jaap S. Sinninghe Damsté
Jaap S. Sinninghe Damsté
Darci Rush
author_sort Nora Richter
collection DOAJ
description Methanotrophs, in particular methane-oxidizing bacteria (MOB), regulate the release of methane from lakes, and often co-occur with methylotrophs that may enhance methane-oxidation rates. Assessing the interaction and physiological status of these two microbial groups is essential for determining the microbial methane buffering capacity of environmental systems. Microbial membrane lipids are commonly used as taxonomic markers of specific microbial groups; however, few studies have characterized the changes of membrane lipids under different environmental conditions. For the case of methane-cycling microorganisms, this could be useful for determining their physiological status and potential methane buffering capacity. Here we investigated the changes in membrane lipids, bacteriohopanepolyols (BHPs) and respiratory quinones, produced by MOB and methylotrophs in an enrichment co-culture that primarily consists of a methanotroph (Methylobacter sp.) and a methylotroph (Methylotenera sp.) enriched from a freshwater lake under different methane concentrations, temperatures, and salinities. To assess whether the lipid response is similar in methanotrophs adapted to extreme environmental conditions, we also characterize the BHP composition and respiratory quinones of a psychrotolerant methanotroph, Methylovulum psychrotolerans, isolated from an Arctic freshwater lake and grown under different temperatures. Notably, in the Methylobacter-Methylotenera enrichment the relative abundance of the BHPs aminobacteriohopanepentol and aminobacteriohopanepolyols with additional modifications to the side chain increased at higher temperatures and salinities, respectively, whereas there was no change in the distribution of respiratory quinones. In contrast, in the Methylovulum psychrotolerans culture, the relative abundance of unsaturated BHPs increased and ubiquinone 8:8 (UQ8:8) decreased at lower temperatures. The distinct changes in lipid composition between the Methylobacter-Methylotenera enrichment and the psychrotolerant methanotroph at different growth temperatures and the ability of the Methylobacter-Methylotenera enrichment to grow at high salinities with a singular BHP distribution, suggests that methane-cycling microbes have unique lipid responses that enable them to grow even under high environmental stress.
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publisher Frontiers Media S.A.
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spelling doaj-art-bae1d2694f6444e6819904887f35a2552025-02-07T17:15:14ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-02-011610.3389/fmicb.2025.15327191532719Methanotroph-methylotroph lipid adaptations to changing environmental conditionsNora Richter0Laura Villanueva1Laura Villanueva2Ellen C. Hopmans3Nicole J. Bale4Jaap S. Sinninghe Damsté5Jaap S. Sinninghe Damsté6Darci Rush7Department of Marine Microbiology and Biogeochemistry, NIOZ Royal Netherlands Institute for Sea Research, Den Burg, NetherlandsDepartment of Marine Microbiology and Biogeochemistry, NIOZ Royal Netherlands Institute for Sea Research, Den Burg, NetherlandsDepartment of Biology, Faculty of Science, Utrecht University, Utrecht, NetherlandsDepartment of Marine Microbiology and Biogeochemistry, NIOZ Royal Netherlands Institute for Sea Research, Den Burg, NetherlandsDepartment of Marine Microbiology and Biogeochemistry, NIOZ Royal Netherlands Institute for Sea Research, Den Burg, NetherlandsDepartment of Marine Microbiology and Biogeochemistry, NIOZ Royal Netherlands Institute for Sea Research, Den Burg, NetherlandsDepartment of Earth Sciences, Faculty of Geosciences, Utrecht University, Utrecht, NetherlandsDepartment of Marine Microbiology and Biogeochemistry, NIOZ Royal Netherlands Institute for Sea Research, Den Burg, NetherlandsMethanotrophs, in particular methane-oxidizing bacteria (MOB), regulate the release of methane from lakes, and often co-occur with methylotrophs that may enhance methane-oxidation rates. Assessing the interaction and physiological status of these two microbial groups is essential for determining the microbial methane buffering capacity of environmental systems. Microbial membrane lipids are commonly used as taxonomic markers of specific microbial groups; however, few studies have characterized the changes of membrane lipids under different environmental conditions. For the case of methane-cycling microorganisms, this could be useful for determining their physiological status and potential methane buffering capacity. Here we investigated the changes in membrane lipids, bacteriohopanepolyols (BHPs) and respiratory quinones, produced by MOB and methylotrophs in an enrichment co-culture that primarily consists of a methanotroph (Methylobacter sp.) and a methylotroph (Methylotenera sp.) enriched from a freshwater lake under different methane concentrations, temperatures, and salinities. To assess whether the lipid response is similar in methanotrophs adapted to extreme environmental conditions, we also characterize the BHP composition and respiratory quinones of a psychrotolerant methanotroph, Methylovulum psychrotolerans, isolated from an Arctic freshwater lake and grown under different temperatures. Notably, in the Methylobacter-Methylotenera enrichment the relative abundance of the BHPs aminobacteriohopanepentol and aminobacteriohopanepolyols with additional modifications to the side chain increased at higher temperatures and salinities, respectively, whereas there was no change in the distribution of respiratory quinones. In contrast, in the Methylovulum psychrotolerans culture, the relative abundance of unsaturated BHPs increased and ubiquinone 8:8 (UQ8:8) decreased at lower temperatures. The distinct changes in lipid composition between the Methylobacter-Methylotenera enrichment and the psychrotolerant methanotroph at different growth temperatures and the ability of the Methylobacter-Methylotenera enrichment to grow at high salinities with a singular BHP distribution, suggests that methane-cycling microbes have unique lipid responses that enable them to grow even under high environmental stress.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1532719/fullbacteriohopanepolyolsmethane-oxidizing bacteriarespiratory quinonesmembrane lipidsmethylotroph
spellingShingle Nora Richter
Laura Villanueva
Laura Villanueva
Ellen C. Hopmans
Nicole J. Bale
Jaap S. Sinninghe Damsté
Jaap S. Sinninghe Damsté
Darci Rush
Methanotroph-methylotroph lipid adaptations to changing environmental conditions
Frontiers in Microbiology
bacteriohopanepolyols
methane-oxidizing bacteria
respiratory quinones
membrane lipids
methylotroph
title Methanotroph-methylotroph lipid adaptations to changing environmental conditions
title_full Methanotroph-methylotroph lipid adaptations to changing environmental conditions
title_fullStr Methanotroph-methylotroph lipid adaptations to changing environmental conditions
title_full_unstemmed Methanotroph-methylotroph lipid adaptations to changing environmental conditions
title_short Methanotroph-methylotroph lipid adaptations to changing environmental conditions
title_sort methanotroph methylotroph lipid adaptations to changing environmental conditions
topic bacteriohopanepolyols
methane-oxidizing bacteria
respiratory quinones
membrane lipids
methylotroph
url https://www.frontiersin.org/articles/10.3389/fmicb.2025.1532719/full
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AT lauravillanueva methanotrophmethylotrophlipidadaptationstochangingenvironmentalconditions
AT ellenchopmans methanotrophmethylotrophlipidadaptationstochangingenvironmentalconditions
AT nicolejbale methanotrophmethylotrophlipidadaptationstochangingenvironmentalconditions
AT jaapssinninghedamste methanotrophmethylotrophlipidadaptationstochangingenvironmentalconditions
AT jaapssinninghedamste methanotrophmethylotrophlipidadaptationstochangingenvironmentalconditions
AT darcirush methanotrophmethylotrophlipidadaptationstochangingenvironmentalconditions