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

Carrion Fonseca, Ornella, Todd, Jonathan, Curson, Andrew, Walsham, Keanu, Zhu, Xiaoyu and Monaco, Serena (2023) DMSOP-cleaving enzymes are diverse and widely distributed in marine microorganisms. Nature Microbiology, 8 (12). pp. 2326-2337. ISSN 2058-5276

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Abstract

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.

Item Type: Article
Additional Information: Acknowledgements: We thank the staff from the BL18U1 beamline of National Facility for Protein Sciences Shanghai (NFPS) and Shanghai Synchrotron Radiation Facility for assistance during data collection. We thank P. Nicholson and R. Payet for providing Fusarium culmorum Fu42 and saltmarsh sediment samples, respectively. We also thank the late D. Tawfik at the Weizmann Institute of Science for providing Br–DMSP. This work was supported by the National Key R and D Program of China (2022YFC2807500 and 2021YFA0909600), the National Science Foundation of China (92251303, 42276102, 42076229, 42106142 and 31961133016), the Fundamental Research Funds for the Central Universities (202041011 and 202172002), Major Scientific and Technological Innovation Project (MSTIP) of Shandong Province (2019JZZY010817), the Taishan Scholars Program of Shandong Province, China (tspd20181203 and tsqn202306092) and the Natural Science Foundation of Shandong Province (ZR2021QD071). Work in S.J.G.’s group was supported by the Simons Foundation International BIOS-SCOPE program. Work in G.P.’s laboratory was funded by the Deutsche Forschungsgemeinschaft (German Research Foundation, DFG) through CRC1127 ChemBioSys (239748522) and EXC 2051 Balance of the Microverse (390713860). Work in J.D.T.’s laboratory was funded by the Natural Environment Research Council (NE/P012671, NE/S001352, NE/V000756/1 and NE/X000990/1) and the Leverhulme trust (RPG-2020-413) grants. K.S.W. was supported by a BBSRC Norwich Research Park Biosciences Doctoral Training Partnership grant (BB/M011216/1).
Uncontrolled Keywords: dimethylsulfoxonium propionate,dimethylsulfoniopropionate,dimethylsulfoxide,dimethylsulfide,dmsp lyases,marine sulfur cycle,applied microbiology and biotechnology,microbiology (medical),genetics,cell biology,microbiology,immunology,sdg 14 - life below water ,/dk/atira/pure/subjectarea/asjc/2400/2402
Faculty \ School: Faculty of Science > School of Biological Sciences
Faculty of Science > School of Pharmacy
UEA Research Groups: Faculty of Science > Research Groups > Molecular Microbiology
Related URLs:
Depositing User: LivePure Connector
Date Deposited: 10 Nov 2023 03:23
Last Modified: 18 Jun 2024 00:17
URI: https://ueaeprints.uea.ac.uk/id/eprint/93617
DOI: 10.1038/s41564-023-01526-4

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