Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Wang, Tao, Huang, Qiuyuan, Burns, Andrew S., Moran, Mary Ann, Whitman, William B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
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
_version_ 1784854479552643072
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
work_keys_str_mv AT wangtao oxidativestressregulatesapivotalmetabolicswitchindimethylsulfoniopropionatedegradationbythemarinebacteriumruegeriapomeroyi
AT huangqiuyuan oxidativestressregulatesapivotalmetabolicswitchindimethylsulfoniopropionatedegradationbythemarinebacteriumruegeriapomeroyi
AT burnsandrews oxidativestressregulatesapivotalmetabolicswitchindimethylsulfoniopropionatedegradationbythemarinebacteriumruegeriapomeroyi
AT moranmaryann oxidativestressregulatesapivotalmetabolicswitchindimethylsulfoniopropionatedegradationbythemarinebacteriumruegeriapomeroyi
AT whitmanwilliamb oxidativestressregulatesapivotalmetabolicswitchindimethylsulfoniopropionatedegradationbythemarinebacteriumruegeriapomeroyi