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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Online Access: | https://doi.org/10.3389/fmicb.2022.958417 https://doaj.org/article/2e93112842b64dd5bb725bfd040ba9a2 |
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ftdoajarticles:oai:doaj.org/article:2e93112842b64dd5bb725bfd040ba9a2 2023-05-15T15:12:44+02:00 Metabolic responses of thermophilic endospores to sudden heat-induced perturbation in marine sediment samples Anirban Chakraborty Jayne E. Rattray Sienna S. Drake Stuart Matthews Carmen Li Bo Barker Jørgensen Casey R. J. Hubert 2022-08-01T00:00:00Z https://doi.org/10.3389/fmicb.2022.958417 https://doaj.org/article/2e93112842b64dd5bb725bfd040ba9a2 EN eng Frontiers Media S.A. https://www.frontiersin.org/articles/10.3389/fmicb.2022.958417/full https://doaj.org/toc/1664-302X 1664-302X doi:10.3389/fmicb.2022.958417 https://doaj.org/article/2e93112842b64dd5bb725bfd040ba9a2 Frontiers in Microbiology, Vol 13 (2022) thermophiles endospores dormancy metabolomics sediment microbiome Microbiology QR1-502 article 2022 ftdoajarticles https://doi.org/10.3389/fmicb.2022.958417 2022-12-31T00:54:37Z 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 ... Article in Journal/Newspaper Arctic Directory of Open Access Journals: DOAJ Articles Arctic Frontiers in Microbiology 13 |
institution |
Open Polar |
collection |
Directory of Open Access Journals: DOAJ Articles |
op_collection_id |
ftdoajarticles |
language |
English |
topic |
thermophiles endospores dormancy metabolomics sediment microbiome Microbiology QR1-502 |
spellingShingle |
thermophiles endospores dormancy metabolomics sediment microbiome Microbiology QR1-502 Anirban Chakraborty Jayne E. Rattray Sienna S. Drake Stuart Matthews Carmen Li Bo Barker Jørgensen Casey R. J. Hubert Metabolic responses of thermophilic endospores to sudden heat-induced perturbation in marine sediment samples |
topic_facet |
thermophiles endospores dormancy metabolomics sediment microbiome Microbiology QR1-502 |
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 ... |
format |
Article in Journal/Newspaper |
author |
Anirban Chakraborty Jayne E. Rattray Sienna S. Drake Stuart Matthews Carmen Li Bo Barker Jørgensen Casey R. J. Hubert |
author_facet |
Anirban Chakraborty Jayne E. Rattray Sienna S. Drake Stuart Matthews Carmen Li Bo Barker Jørgensen Casey R. J. Hubert |
author_sort |
Anirban Chakraborty |
title |
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_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_sort |
metabolic responses of thermophilic endospores to sudden heat-induced perturbation in marine sediment samples |
publisher |
Frontiers Media S.A. |
publishDate |
2022 |
url |
https://doi.org/10.3389/fmicb.2022.958417 https://doaj.org/article/2e93112842b64dd5bb725bfd040ba9a2 |
geographic |
Arctic |
geographic_facet |
Arctic |
genre |
Arctic |
genre_facet |
Arctic |
op_source |
Frontiers in Microbiology, Vol 13 (2022) |
op_relation |
https://www.frontiersin.org/articles/10.3389/fmicb.2022.958417/full https://doaj.org/toc/1664-302X 1664-302X doi:10.3389/fmicb.2022.958417 https://doaj.org/article/2e93112842b64dd5bb725bfd040ba9a2 |
op_doi |
https://doi.org/10.3389/fmicb.2022.958417 |
container_title |
Frontiers in Microbiology |
container_volume |
13 |
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1766343371796774912 |