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Metabolic responses of thermophilic endospores to sudden heat-induced perturbation in marine sediment samples

Microbially mediated processes in a given habitat tend to be catalyzed by abundant populations that are ecologically adapted to exploit specific environmental characteristics. Typically, metabolic activities of rare populations are limited but may be stimulated in response to acute environmental str...

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Detalles Bibliográficos
Autores principales: Chakraborty, Anirban, Rattray, Jayne E., Drake, Sienna S., Matthews, Stuart, Li, Carmen, Jørgensen, Bo Barker, Hubert, Casey R. J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9411986/
https://www.ncbi.nlm.nih.gov/pubmed/36033870
http://dx.doi.org/10.3389/fmicb.2022.958417
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author Chakraborty, Anirban
Rattray, Jayne E.
Drake, Sienna S.
Matthews, Stuart
Li, Carmen
Jørgensen, Bo Barker
Hubert, Casey R. J.
author_facet Chakraborty, Anirban
Rattray, Jayne E.
Drake, Sienna S.
Matthews, Stuart
Li, Carmen
Jørgensen, Bo Barker
Hubert, Casey R. J.
author_sort Chakraborty, Anirban
collection PubMed
description Microbially mediated processes in a given habitat tend to be catalyzed by abundant populations that are ecologically adapted to exploit specific environmental characteristics. Typically, metabolic activities of rare populations are limited but may be stimulated in response to acute environmental stressors. Community responses to sudden changes in temperature and pressure can include suppression and activation of different populations, but these dynamics remain poorly understood. The permanently cold ocean floor hosts countless low-abundance microbes including endospores of thermophilic bacteria. Incubating sediments at high temperature resuscitates viable spores, causing the proliferation of bacterial populations. This presents a tractable system for investigating changes in a microbiome's community structure in response to dramatic environmental perturbations. Incubating permanently cold Arctic fjord sediments at 50°C for 216 h with and without volatile fatty acid amendment provoked major changes in community structure. Germination of thermophilic spores from the sediment rare biosphere was tracked using mass spectrometry-based metabolomics, radiotracer-based sulfate reduction rate measurements, and high-throughput 16S rRNA gene sequencing. Comparing community similarity at different intervals of the incubations showed distinct temporal shifts in microbial populations, depending on organic substrate amendment. Metabolite patterns indicated that amino acids and other sediment-derived organics were decomposed by fermentative Clostridia within the first 12–48 h. This fueled early and late phases of exponential increases in sulfate reduction, highlighting the cross-feeding of volatile fatty acids as electron donors for different sulfate-reducing Desulfotomaculia populations. The succession of germinated endospores triggered by sudden exposure to high temperature and controlled by nutrient availability offers a model for understanding the ecological response of dormant microbial communities following major environmental perturbations.
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spelling pubmed-94119862022-08-27 Metabolic responses of thermophilic endospores to sudden heat-induced perturbation in marine sediment samples Chakraborty, Anirban Rattray, Jayne E. Drake, Sienna S. Matthews, Stuart Li, Carmen Jørgensen, Bo Barker Hubert, Casey R. J. Front Microbiol Microbiology Microbially mediated processes in a given habitat tend to be catalyzed by abundant populations that are ecologically adapted to exploit specific environmental characteristics. Typically, metabolic activities of rare populations are limited but may be stimulated in response to acute environmental stressors. Community responses to sudden changes in temperature and pressure can include suppression and activation of different populations, but these dynamics remain poorly understood. The permanently cold ocean floor hosts countless low-abundance microbes including endospores of thermophilic bacteria. Incubating sediments at high temperature resuscitates viable spores, causing the proliferation of bacterial populations. This presents a tractable system for investigating changes in a microbiome's community structure in response to dramatic environmental perturbations. Incubating permanently cold Arctic fjord sediments at 50°C for 216 h with and without volatile fatty acid amendment provoked major changes in community structure. Germination of thermophilic spores from the sediment rare biosphere was tracked using mass spectrometry-based metabolomics, radiotracer-based sulfate reduction rate measurements, and high-throughput 16S rRNA gene sequencing. Comparing community similarity at different intervals of the incubations showed distinct temporal shifts in microbial populations, depending on organic substrate amendment. Metabolite patterns indicated that amino acids and other sediment-derived organics were decomposed by fermentative Clostridia within the first 12–48 h. This fueled early and late phases of exponential increases in sulfate reduction, highlighting the cross-feeding of volatile fatty acids as electron donors for different sulfate-reducing Desulfotomaculia populations. The succession of germinated endospores triggered by sudden exposure to high temperature and controlled by nutrient availability offers a model for understanding the ecological response of dormant microbial communities following major environmental perturbations. Frontiers Media S.A. 2022-08-12 /pmc/articles/PMC9411986/ /pubmed/36033870 http://dx.doi.org/10.3389/fmicb.2022.958417 Text en Copyright © 2022 Chakraborty, Rattray, Drake, Matthews, Li, Jørgensen and Hubert. https://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
Chakraborty, Anirban
Rattray, Jayne E.
Drake, Sienna S.
Matthews, Stuart
Li, Carmen
Jørgensen, Bo Barker
Hubert, Casey R. J.
Metabolic responses of thermophilic endospores to sudden heat-induced perturbation in marine sediment samples
title Metabolic responses of thermophilic endospores to sudden heat-induced perturbation in marine sediment samples
title_full Metabolic responses of thermophilic endospores to sudden heat-induced perturbation in marine sediment samples
title_fullStr Metabolic responses of thermophilic endospores to sudden heat-induced perturbation in marine sediment samples
title_full_unstemmed Metabolic responses of thermophilic endospores to sudden heat-induced perturbation in marine sediment samples
title_short Metabolic responses of thermophilic endospores to sudden heat-induced perturbation in marine sediment samples
title_sort metabolic responses of thermophilic endospores to sudden heat-induced perturbation in marine sediment samples
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9411986/
https://www.ncbi.nlm.nih.gov/pubmed/36033870
http://dx.doi.org/10.3389/fmicb.2022.958417
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