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Oxidative Stress Regulates a Pivotal Metabolic Switch in Dimethylsulfoniopropionate Degradation by the Marine Bacterium Ruegeria pomeroyi
Dimethylsulfoniopropionate (DMSP) is an abundant organic compound in marine surface water and source of dimethyl sulfide (DMS), the largest natural sulfur source to the upper atmosphere. Marine bacteria either mineralize DMSP through the demethylation pathway or transform it to DMS through the cleav...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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American Society for Microbiology
2022
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769926/ https://www.ncbi.nlm.nih.gov/pubmed/36301115 http://dx.doi.org/10.1128/spectrum.03191-22 |
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author | Wang, Tao Huang, Qiuyuan Burns, Andrew S. Moran, Mary Ann Whitman, William B. |
author_facet | Wang, Tao Huang, Qiuyuan Burns, Andrew S. Moran, Mary Ann Whitman, William B. |
author_sort | Wang, Tao |
collection | PubMed |
description | Dimethylsulfoniopropionate (DMSP) is an abundant organic compound in marine surface water and source of dimethyl sulfide (DMS), the largest natural sulfur source to the upper atmosphere. Marine bacteria either mineralize DMSP through the demethylation pathway or transform it to DMS through the cleavage pathway. Factors that regulate which pathway is utilized are not fully understood. In chemostat experiments, the marine Roseobacter Ruegeria pomeroyi DSS-3 was exposed to oxidative stress either during growth with H(2)O(2) or by mutation of the gene encoding catalase. Oxidative stress reduced expression of the genes in the demethylation pathway and increased expression of those encoding the cleavage pathway. These results are contrary to the sulfur demand hypothesis, which theorizes that DMSP metabolism is driven by sulfur requirements of bacterial cells. Instead, we find strong evidence consistent with oxidative stress control over the switch in DMSP metabolism from demethylation to DMS production in an ecologically relevant marine bacterium. IMPORTANCE Dimethylsulfoniopropionate (DMSP) is the most abundant low-molecular-weight organic compound in marine surface water and source of dimethyl sulfide (DMS), a climatically active gas that connects the marine and terrestrial sulfur cycles. Marine bacteria are the major DMSP consumers, either generating DMS or consuming DMSP as a source of reduced carbon and sulfur. However, the factors regulating the DMSP catabolism in bacteria are not well understood. Marine bacteria are also exposed to oxidative stress. RNA sequencing (RNA-seq) experiments showed that oxidative stress induced in the laboratory reduced expression of the genes encoding the consumption of DMSP via the demethylation pathway and increased the expression of genes encoding DMS production via the cleavage pathway in the marine bacterium Ruegeria pomeroyi. These results support a model where DMS production in the ocean is regulated in part by oxidative stress. |
format | Online Article Text |
id | pubmed-9769926 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-97699262022-12-22 Oxidative Stress Regulates a Pivotal Metabolic Switch in Dimethylsulfoniopropionate Degradation by the Marine Bacterium Ruegeria pomeroyi Wang, Tao Huang, Qiuyuan Burns, Andrew S. Moran, Mary Ann Whitman, William B. Microbiol Spectr Research Article Dimethylsulfoniopropionate (DMSP) is an abundant organic compound in marine surface water and source of dimethyl sulfide (DMS), the largest natural sulfur source to the upper atmosphere. Marine bacteria either mineralize DMSP through the demethylation pathway or transform it to DMS through the cleavage pathway. Factors that regulate which pathway is utilized are not fully understood. In chemostat experiments, the marine Roseobacter Ruegeria pomeroyi DSS-3 was exposed to oxidative stress either during growth with H(2)O(2) or by mutation of the gene encoding catalase. Oxidative stress reduced expression of the genes in the demethylation pathway and increased expression of those encoding the cleavage pathway. These results are contrary to the sulfur demand hypothesis, which theorizes that DMSP metabolism is driven by sulfur requirements of bacterial cells. Instead, we find strong evidence consistent with oxidative stress control over the switch in DMSP metabolism from demethylation to DMS production in an ecologically relevant marine bacterium. IMPORTANCE Dimethylsulfoniopropionate (DMSP) is the most abundant low-molecular-weight organic compound in marine surface water and source of dimethyl sulfide (DMS), a climatically active gas that connects the marine and terrestrial sulfur cycles. Marine bacteria are the major DMSP consumers, either generating DMS or consuming DMSP as a source of reduced carbon and sulfur. However, the factors regulating the DMSP catabolism in bacteria are not well understood. Marine bacteria are also exposed to oxidative stress. RNA sequencing (RNA-seq) experiments showed that oxidative stress induced in the laboratory reduced expression of the genes encoding the consumption of DMSP via the demethylation pathway and increased the expression of genes encoding DMS production via the cleavage pathway in the marine bacterium Ruegeria pomeroyi. These results support a model where DMS production in the ocean is regulated in part by oxidative stress. American Society for Microbiology 2022-10-27 /pmc/articles/PMC9769926/ /pubmed/36301115 http://dx.doi.org/10.1128/spectrum.03191-22 Text en Copyright © 2022 Wang et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Article Wang, Tao Huang, Qiuyuan Burns, Andrew S. Moran, Mary Ann Whitman, William B. Oxidative Stress Regulates a Pivotal Metabolic Switch in Dimethylsulfoniopropionate Degradation by the Marine Bacterium Ruegeria pomeroyi |
title | Oxidative Stress Regulates a Pivotal Metabolic Switch in Dimethylsulfoniopropionate Degradation by the Marine Bacterium Ruegeria pomeroyi |
title_full | Oxidative Stress Regulates a Pivotal Metabolic Switch in Dimethylsulfoniopropionate Degradation by the Marine Bacterium Ruegeria pomeroyi |
title_fullStr | Oxidative Stress Regulates a Pivotal Metabolic Switch in Dimethylsulfoniopropionate Degradation by the Marine Bacterium Ruegeria pomeroyi |
title_full_unstemmed | Oxidative Stress Regulates a Pivotal Metabolic Switch in Dimethylsulfoniopropionate Degradation by the Marine Bacterium Ruegeria pomeroyi |
title_short | Oxidative Stress Regulates a Pivotal Metabolic Switch in Dimethylsulfoniopropionate Degradation by the Marine Bacterium Ruegeria pomeroyi |
title_sort | oxidative stress regulates a pivotal metabolic switch in dimethylsulfoniopropionate degradation by the marine bacterium ruegeria pomeroyi |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769926/ https://www.ncbi.nlm.nih.gov/pubmed/36301115 http://dx.doi.org/10.1128/spectrum.03191-22 |
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