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DMSOP-cleaving enzymes are diverse and widely distributed in marine microorganisms

Dimethylsulfoxonium propionate (DMSOP) is a recently identified and abundant marine organosulfur compound with roles in oxidative stress protection, global carbon and sulfur cycling and, as shown here, potentially in osmotolerance. Microbial DMSOP cleavage yields dimethyl sulfoxide, a ubiquitous mar...

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Autores principales: Carrión, Ornella, Li, Chun-Yang, Peng, Ming, Wang, Jinyan, Pohnert, Georg, Azizah, Muhaiminatul, Zhu, Xiao-Yu, Curson, Andrew R. J., Wang, Qing, Walsham, Keanu S., Zhang, Xiao-Hua, Monaco, Serena, Harvey, James M., Chen, Xiu-Lan, Gao, Chao, Wang, Ning, Wang, Xiu-Juan, Wang, Peng, Giovanonni, Stephen J., Lee, Chih-Ping, Suffridge, Christopher P., Zhang, Yu, Luo, Ziqi, Wang, Dazhi, Todd, Jonathan D., Zhang, Yu-Zhong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10686828/
https://www.ncbi.nlm.nih.gov/pubmed/38030907
http://dx.doi.org/10.1038/s41564-023-01526-4
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author Carrión, Ornella
Li, Chun-Yang
Peng, Ming
Wang, Jinyan
Pohnert, Georg
Azizah, Muhaiminatul
Zhu, Xiao-Yu
Curson, Andrew R. J.
Wang, Qing
Walsham, Keanu S.
Zhang, Xiao-Hua
Monaco, Serena
Harvey, James M.
Chen, Xiu-Lan
Gao, Chao
Wang, Ning
Wang, Xiu-Juan
Wang, Peng
Giovanonni, Stephen J.
Lee, Chih-Ping
Suffridge, Christopher P.
Zhang, Yu
Luo, Ziqi
Wang, Dazhi
Todd, Jonathan D.
Zhang, Yu-Zhong
author_facet Carrión, Ornella
Li, Chun-Yang
Peng, Ming
Wang, Jinyan
Pohnert, Georg
Azizah, Muhaiminatul
Zhu, Xiao-Yu
Curson, Andrew R. J.
Wang, Qing
Walsham, Keanu S.
Zhang, Xiao-Hua
Monaco, Serena
Harvey, James M.
Chen, Xiu-Lan
Gao, Chao
Wang, Ning
Wang, Xiu-Juan
Wang, Peng
Giovanonni, Stephen J.
Lee, Chih-Ping
Suffridge, Christopher P.
Zhang, Yu
Luo, Ziqi
Wang, Dazhi
Todd, Jonathan D.
Zhang, Yu-Zhong
author_sort Carrión, Ornella
collection PubMed
description Dimethylsulfoxonium propionate (DMSOP) is a recently identified and abundant marine organosulfur compound with roles in oxidative stress protection, global carbon and sulfur cycling and, as shown here, potentially in osmotolerance. Microbial DMSOP cleavage yields dimethyl sulfoxide, a ubiquitous marine metabolite, and acrylate, but the enzymes responsible, and their environmental importance, were unknown. Here we report DMSOP cleavage mechanisms in diverse heterotrophic bacteria, fungi and phototrophic algae not previously known to have this activity, and highlight the unappreciated importance of this process in marine sediment environments. These diverse organisms, including Roseobacter, SAR11 bacteria and Emiliania huxleyi, utilized their dimethylsulfoniopropionate lyase ‘Ddd’ or ‘Alma’ enzymes to cleave DMSOP via similar catalytic mechanisms to those for dimethylsulfoniopropionate. Given the annual teragram predictions for DMSOP production and its prevalence in marine sediments, our results highlight that DMSOP cleavage is likely a globally significant process influencing carbon and sulfur fluxes and ecological interactions.
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spelling pubmed-106868282023-12-01 DMSOP-cleaving enzymes are diverse and widely distributed in marine microorganisms Carrión, Ornella Li, Chun-Yang Peng, Ming Wang, Jinyan Pohnert, Georg Azizah, Muhaiminatul Zhu, Xiao-Yu Curson, Andrew R. J. Wang, Qing Walsham, Keanu S. Zhang, Xiao-Hua Monaco, Serena Harvey, James M. Chen, Xiu-Lan Gao, Chao Wang, Ning Wang, Xiu-Juan Wang, Peng Giovanonni, Stephen J. Lee, Chih-Ping Suffridge, Christopher P. Zhang, Yu Luo, Ziqi Wang, Dazhi Todd, Jonathan D. Zhang, Yu-Zhong Nat Microbiol Article Dimethylsulfoxonium propionate (DMSOP) is a recently identified and abundant marine organosulfur compound with roles in oxidative stress protection, global carbon and sulfur cycling and, as shown here, potentially in osmotolerance. Microbial DMSOP cleavage yields dimethyl sulfoxide, a ubiquitous marine metabolite, and acrylate, but the enzymes responsible, and their environmental importance, were unknown. Here we report DMSOP cleavage mechanisms in diverse heterotrophic bacteria, fungi and phototrophic algae not previously known to have this activity, and highlight the unappreciated importance of this process in marine sediment environments. These diverse organisms, including Roseobacter, SAR11 bacteria and Emiliania huxleyi, utilized their dimethylsulfoniopropionate lyase ‘Ddd’ or ‘Alma’ enzymes to cleave DMSOP via similar catalytic mechanisms to those for dimethylsulfoniopropionate. Given the annual teragram predictions for DMSOP production and its prevalence in marine sediments, our results highlight that DMSOP cleavage is likely a globally significant process influencing carbon and sulfur fluxes and ecological interactions. Nature Publishing Group UK 2023-11-29 2023 /pmc/articles/PMC10686828/ /pubmed/38030907 http://dx.doi.org/10.1038/s41564-023-01526-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Carrión, Ornella
Li, Chun-Yang
Peng, Ming
Wang, Jinyan
Pohnert, Georg
Azizah, Muhaiminatul
Zhu, Xiao-Yu
Curson, Andrew R. J.
Wang, Qing
Walsham, Keanu S.
Zhang, Xiao-Hua
Monaco, Serena
Harvey, James M.
Chen, Xiu-Lan
Gao, Chao
Wang, Ning
Wang, Xiu-Juan
Wang, Peng
Giovanonni, Stephen J.
Lee, Chih-Ping
Suffridge, Christopher P.
Zhang, Yu
Luo, Ziqi
Wang, Dazhi
Todd, Jonathan D.
Zhang, Yu-Zhong
DMSOP-cleaving enzymes are diverse and widely distributed in marine microorganisms
title DMSOP-cleaving enzymes are diverse and widely distributed in marine microorganisms
title_full DMSOP-cleaving enzymes are diverse and widely distributed in marine microorganisms
title_fullStr DMSOP-cleaving enzymes are diverse and widely distributed in marine microorganisms
title_full_unstemmed DMSOP-cleaving enzymes are diverse and widely distributed in marine microorganisms
title_short DMSOP-cleaving enzymes are diverse and widely distributed in marine microorganisms
title_sort dmsop-cleaving enzymes are diverse and widely distributed in marine microorganisms
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10686828/
https://www.ncbi.nlm.nih.gov/pubmed/38030907
http://dx.doi.org/10.1038/s41564-023-01526-4
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