Interplay between autotrophic and heterotrophic prokaryotic metabolism in the bathypelagic realm revealed by metatranscriptomic analyses

Background Heterotrophic microbes inhabiting the dark ocean largely depend on the settling of organic matter from the sunlit ocean. However, this sinking of organic materials is insufficient to cover their demand for energy and alternative sources such as chemoautotrophy have been proposed. Reduced...

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Published in:Microbiome
Main Authors: Srivastava, A., De Corte, D., Garcia, J.A.L., Swan, B.K., Stepanauskas, R., Herndl, G., Sintes, E.
Format: Article in Journal/Newspaper
Language:English
Published: 2023
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Online Access:https://www.vliz.be/imisdocs/publications/41/395441.pdf
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spelling ftnioz:oai:imis.nioz.nl:381106 2024-09-15T18:17:18+00:00 Interplay between autotrophic and heterotrophic prokaryotic metabolism in the bathypelagic realm revealed by metatranscriptomic analyses Srivastava, A. De Corte, D. Garcia, J.A.L. Swan, B.K. Stepanauskas, R. Herndl, G. Sintes, E. 2023 application/pdf https://www.vliz.be/imisdocs/publications/41/395441.pdf en eng info:eu-repo/semantics/altIdentifier/wos/001103544400001 info:eu-repo/semantics/altIdentifier/doi/doi.org/10.1186/s40168-023-01688-7 https://www.vliz.be/imisdocs/publications/41/395441.pdf info:eu-repo/semantics/openAccess %3Ci%3EEnvironmental+Microbiome+11%281%29%3C%2Fi%3E%3A+239.+%3Ca+href%3D%22https%3A%2F%2Fdx.doi.org%2F10.1186%2Fs40168-023-01688-7%22+target%3D%22_blank%22%3Ehttps%3A%2F%2Fdx.doi.org%2F10.1186%2Fs40168-023-01688-7%3C%2Fa%3E info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion 2023 ftnioz https://doi.org/10.1186/s40168-023-01688-7 2024-08-26T03:37:14Z Background Heterotrophic microbes inhabiting the dark ocean largely depend on the settling of organic matter from the sunlit ocean. However, this sinking of organic materials is insufficient to cover their demand for energy and alternative sources such as chemoautotrophy have been proposed. Reduced sulfur compounds, such as thiosulfate, are a potential energy source for both auto- and heterotrophic marine prokaryotes. Methods Seawater samples were collected from Labrador Sea Water (LSW, ~ 2000m depth) in the North Atlantic and incubated in the dark at in situ temperature unamended, amended with 1µM thiosulfate, or with 1µM thiosulfate plus 10µM glucose and 10µM acetate (thiosulfate plus dissolved organic matter, DOM). Inorganic carbon fixation was measured in the different treatments and samples for metatranscriptomic analyses were collected after 1h and 72h of incubation. Results Amendment of LSW with thiosulfate and thiosulfate plus DOM enhanced prokaryotic inorganic carbon fixation. The energy generated via chemoautotrophy and heterotrophy in the amended prokaryotic communities was used for the biosynthesis of glycogen and phospholipids as storage molecules. The addition of thiosulfate stimulated unclassified bacteria, sulfur-oxidizing Deltaproteobacteria (SAR324 cluster bacteria), Epsilonproteobacteria ( Sulfurimonas sp.), and Gammaproteobacteria (SUP05 cluster bacteria), whereas, the amendment with thiosulfate plus DOM stimulated typically copiotrophic Gammaproteobacteria (closely related to Vibrio sp. and Pseudoalteromonas sp.). Conclusions The gene expression pattern of thiosulfate utilizing microbes specifically of genes involved in energy production via sulfur oxidation and coupled to CO 2 fixation pathways coincided with the change in the transcriptional profile of the heterotrophic prokaryotic community (genes involved in promoting energy storage), suggesting a fine-tuned metabolic interplay between chemoautotrophic and heterotrophic microbes in the dark ocean. Article in Journal/Newspaper Labrador Sea North Atlantic NIOZ Repository (Royal Netherlands Institute for Sea Research) Microbiome 11 1
institution Open Polar
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language English
description Background Heterotrophic microbes inhabiting the dark ocean largely depend on the settling of organic matter from the sunlit ocean. However, this sinking of organic materials is insufficient to cover their demand for energy and alternative sources such as chemoautotrophy have been proposed. Reduced sulfur compounds, such as thiosulfate, are a potential energy source for both auto- and heterotrophic marine prokaryotes. Methods Seawater samples were collected from Labrador Sea Water (LSW, ~ 2000m depth) in the North Atlantic and incubated in the dark at in situ temperature unamended, amended with 1µM thiosulfate, or with 1µM thiosulfate plus 10µM glucose and 10µM acetate (thiosulfate plus dissolved organic matter, DOM). Inorganic carbon fixation was measured in the different treatments and samples for metatranscriptomic analyses were collected after 1h and 72h of incubation. Results Amendment of LSW with thiosulfate and thiosulfate plus DOM enhanced prokaryotic inorganic carbon fixation. The energy generated via chemoautotrophy and heterotrophy in the amended prokaryotic communities was used for the biosynthesis of glycogen and phospholipids as storage molecules. The addition of thiosulfate stimulated unclassified bacteria, sulfur-oxidizing Deltaproteobacteria (SAR324 cluster bacteria), Epsilonproteobacteria ( Sulfurimonas sp.), and Gammaproteobacteria (SUP05 cluster bacteria), whereas, the amendment with thiosulfate plus DOM stimulated typically copiotrophic Gammaproteobacteria (closely related to Vibrio sp. and Pseudoalteromonas sp.). Conclusions The gene expression pattern of thiosulfate utilizing microbes specifically of genes involved in energy production via sulfur oxidation and coupled to CO 2 fixation pathways coincided with the change in the transcriptional profile of the heterotrophic prokaryotic community (genes involved in promoting energy storage), suggesting a fine-tuned metabolic interplay between chemoautotrophic and heterotrophic microbes in the dark ocean.
format Article in Journal/Newspaper
author Srivastava, A.
De Corte, D.
Garcia, J.A.L.
Swan, B.K.
Stepanauskas, R.
Herndl, G.
Sintes, E.
spellingShingle Srivastava, A.
De Corte, D.
Garcia, J.A.L.
Swan, B.K.
Stepanauskas, R.
Herndl, G.
Sintes, E.
Interplay between autotrophic and heterotrophic prokaryotic metabolism in the bathypelagic realm revealed by metatranscriptomic analyses
author_facet Srivastava, A.
De Corte, D.
Garcia, J.A.L.
Swan, B.K.
Stepanauskas, R.
Herndl, G.
Sintes, E.
author_sort Srivastava, A.
title Interplay between autotrophic and heterotrophic prokaryotic metabolism in the bathypelagic realm revealed by metatranscriptomic analyses
title_short Interplay between autotrophic and heterotrophic prokaryotic metabolism in the bathypelagic realm revealed by metatranscriptomic analyses
title_full Interplay between autotrophic and heterotrophic prokaryotic metabolism in the bathypelagic realm revealed by metatranscriptomic analyses
title_fullStr Interplay between autotrophic and heterotrophic prokaryotic metabolism in the bathypelagic realm revealed by metatranscriptomic analyses
title_full_unstemmed Interplay between autotrophic and heterotrophic prokaryotic metabolism in the bathypelagic realm revealed by metatranscriptomic analyses
title_sort interplay between autotrophic and heterotrophic prokaryotic metabolism in the bathypelagic realm revealed by metatranscriptomic analyses
publishDate 2023
url https://www.vliz.be/imisdocs/publications/41/395441.pdf
genre Labrador Sea
North Atlantic
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North Atlantic
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