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Copiotrophy in a Marine-Biofilm-Derived Roseobacteraceae Bacterium Can Be Supported by Amino Acid Metabolism and Thiosulfate Oxidation

Copiotrophic bacteria that respond rapidly to nutrient availability, particularly high concentrations of carbon sources, play indispensable roles in marine carbon cycling. However, the molecular and metabolic mechanisms governing their response to carbon concentration gradients are not well understo...

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Detalles Bibliográficos
Autores principales: Su, Xiaoyan, Cui, Han, Zhang, Weipeng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10218387/
https://www.ncbi.nlm.nih.gov/pubmed/37239957
http://dx.doi.org/10.3390/ijms24108617
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author Su, Xiaoyan
Cui, Han
Zhang, Weipeng
author_facet Su, Xiaoyan
Cui, Han
Zhang, Weipeng
author_sort Su, Xiaoyan
collection PubMed
description Copiotrophic bacteria that respond rapidly to nutrient availability, particularly high concentrations of carbon sources, play indispensable roles in marine carbon cycling. However, the molecular and metabolic mechanisms governing their response to carbon concentration gradients are not well understood. Here, we focused on a new member of the family Roseobacteraceae isolated from coastal marine biofilms and explored the growth strategy at different carbon concentrations. When cultured in a carbon-rich medium, the bacterium grew to significantly higher cell densities than Ruegeria pomeroyi DSS-3, although there was no difference when cultured in media with reduced carbon. Genomic analysis showed that the bacterium utilized various pathways involved in biofilm formation, amino acid metabolism, and energy production via the oxidation of inorganic sulfur compounds. Transcriptomic analysis indicated that 28.4% of genes were regulated by carbon concentration, with increased carbon concentration inducing the expression of key enzymes in the EMP, ED, PP, and TCA cycles, genes responsible for the transformation of amino acids into TCA intermediates, as well as the sox genes for thiosulfate oxidation. Metabolomics showed that amino acid metabolism was enhanced and preferred in the presence of a high carbon concentration. Mutation of the sox genes decreased cell proton motive force when grown with amino acids and thiosulfate. In conclusion, we propose that copiotrophy in this Roseobacteraceae bacterium can be supported by amino acid metabolism and thiosulfate oxidation.
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spelling pubmed-102183872023-05-27 Copiotrophy in a Marine-Biofilm-Derived Roseobacteraceae Bacterium Can Be Supported by Amino Acid Metabolism and Thiosulfate Oxidation Su, Xiaoyan Cui, Han Zhang, Weipeng Int J Mol Sci Article Copiotrophic bacteria that respond rapidly to nutrient availability, particularly high concentrations of carbon sources, play indispensable roles in marine carbon cycling. However, the molecular and metabolic mechanisms governing their response to carbon concentration gradients are not well understood. Here, we focused on a new member of the family Roseobacteraceae isolated from coastal marine biofilms and explored the growth strategy at different carbon concentrations. When cultured in a carbon-rich medium, the bacterium grew to significantly higher cell densities than Ruegeria pomeroyi DSS-3, although there was no difference when cultured in media with reduced carbon. Genomic analysis showed that the bacterium utilized various pathways involved in biofilm formation, amino acid metabolism, and energy production via the oxidation of inorganic sulfur compounds. Transcriptomic analysis indicated that 28.4% of genes were regulated by carbon concentration, with increased carbon concentration inducing the expression of key enzymes in the EMP, ED, PP, and TCA cycles, genes responsible for the transformation of amino acids into TCA intermediates, as well as the sox genes for thiosulfate oxidation. Metabolomics showed that amino acid metabolism was enhanced and preferred in the presence of a high carbon concentration. Mutation of the sox genes decreased cell proton motive force when grown with amino acids and thiosulfate. In conclusion, we propose that copiotrophy in this Roseobacteraceae bacterium can be supported by amino acid metabolism and thiosulfate oxidation. MDPI 2023-05-11 /pmc/articles/PMC10218387/ /pubmed/37239957 http://dx.doi.org/10.3390/ijms24108617 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Su, Xiaoyan
Cui, Han
Zhang, Weipeng
Copiotrophy in a Marine-Biofilm-Derived Roseobacteraceae Bacterium Can Be Supported by Amino Acid Metabolism and Thiosulfate Oxidation
title Copiotrophy in a Marine-Biofilm-Derived Roseobacteraceae Bacterium Can Be Supported by Amino Acid Metabolism and Thiosulfate Oxidation
title_full Copiotrophy in a Marine-Biofilm-Derived Roseobacteraceae Bacterium Can Be Supported by Amino Acid Metabolism and Thiosulfate Oxidation
title_fullStr Copiotrophy in a Marine-Biofilm-Derived Roseobacteraceae Bacterium Can Be Supported by Amino Acid Metabolism and Thiosulfate Oxidation
title_full_unstemmed Copiotrophy in a Marine-Biofilm-Derived Roseobacteraceae Bacterium Can Be Supported by Amino Acid Metabolism and Thiosulfate Oxidation
title_short Copiotrophy in a Marine-Biofilm-Derived Roseobacteraceae Bacterium Can Be Supported by Amino Acid Metabolism and Thiosulfate Oxidation
title_sort copiotrophy in a marine-biofilm-derived roseobacteraceae bacterium can be supported by amino acid metabolism and thiosulfate oxidation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10218387/
https://www.ncbi.nlm.nih.gov/pubmed/37239957
http://dx.doi.org/10.3390/ijms24108617
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AT cuihan copiotrophyinamarinebiofilmderivedroseobacteraceaebacteriumcanbesupportedbyaminoacidmetabolismandthiosulfateoxidation
AT zhangweipeng copiotrophyinamarinebiofilmderivedroseobacteraceaebacteriumcanbesupportedbyaminoacidmetabolismandthiosulfateoxidation