Mechanistic insights into the key marine dimethylsulfoniopropionate synthesis enzyme DsyB/DSYB

Li, Chun-Yang, Crack, Jason C., Newton-Payne, Simone, Murphy, Andrew R. J., Chen, Xiu-Lan, Pinchbeck, Benjamin J., Zhou, Shun, Williams, Beth T., Peng, Ming, Zhang, Xiao-Hua, Chen, Yin, Le Brun, Nick E., Todd, Jonathan D. and Zhang, Yu-Zhong (2022) Mechanistic insights into the key marine dimethylsulfoniopropionate synthesis enzyme DsyB/DSYB. mLife, 1 (2). pp. 114-130. ISSN 2770-100X

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Abstract

Marine algae and bacteria produce eight billion tonnes of the organosulfur molecule dimethylsulfoniopropionate (DMSP) in Earth’s surface oceans annually. DMSP is an anti-stress compound and, once released into the environment, a major nutrient, signalling molecule and source of climate-active gases. The methionine transamination pathway for DMSP synthesis is used by most known DMSP-producing algae and bacteria. The S-directed S-adenosylmethionine-dependent methyltransferase (SAM-MT) 4-methylthio-2-hydroxybutyrate (MTHB) S-methyltransferase, encoded by the dsyB/DSYB gene, is the key enzyme of this pathway, generating S-adenosylhomocysteine (SAH) and 4-dimethylsulfonio-2-hydroxybutyrate (DMSHB). dsyB/DSYB, present in most haptophyte and dinoflagellate algae with the highest known intracellular DMSP concentrations, is shown to be far more abundant and transcribed in marine environments than any other known DMSP synthesis pathway S-methyltransferase gene. Furthermore, we demonstrate in vitro activity of the bacterial DsyB enzyme from Nisaea denitrificans and provide its crystal structure in complex with SAM and SAH-MTHB, which together provide the first important mechanistic insights into a DMSP synthesis enzyme. Structural and mutational analyses imply that DsyB adopts a proximity and desolvation mechanism for the methyl transfer reaction. Sequence analysis suggests that this mechanism is common to all bacterial DsyB enzymes and also, importantly, eukaryotic DSYB enzymes from e.g., algae that are the major DMSP producers in Earth’s surface oceans.   Impact Statement Dimethylsulfoniopropionate (DMSP) is one of Earth’s most abundant organosulfur containing molecules which influences marine nutrient cycling, chemotaxis, atmospheric chemistry and potentially the climate. This study provides the first structural and mechanistic understanding of the key DMSP synthesis enzyme in marine bacteria (DsyB) and algae (DSYB) that are responsible for the annual production of > 8 billion tonnes of DMSP. DsyB is the first DMSP synthesis enzyme to be analyzed at the structural and mechanistic level. This study defines functional characteristics of the DsyB/DSYB enzyme family that has a central role in driving marine microbial cycling of organosulfur.

Item Type: Article
Additional Information: ACKNOWLEDGMENTS: We thank the staff from BL18U1&BL19U1 beamlines of the National Facility for Protein Sciences Shanghai (NFPS) and Shanghai Synchrotron Radiation Facility, for assistance during data collection. This work was supported by: the National Science Foundation of China (grants 91851205, 42076229, 31961133016), the National Key Research and Development Program of China (2021YFA0909600), the Fundamental Research Funds for the Central Universities (202172002, 202041011), the Major Scientific and Technological Innovation Project (MSTIP) of Shandong Province (2019JZZY010817), the Program of Shandong for Taishan Scholars (tspd20181203), the grant of Laboratory for Marine Biology and Biotechnology (OF2019NO02), Pilot National Laboratory for Marine Science and Technology (Qingdao), the United Kingdom’s Natural and Environmental Research Council (NERC, NE/P012671/1 and NE/N002385/1), and the United Kingdom’s Biotechnology and Biological Sciences Research Council (BBSRC, BB/P006140/1).
Uncontrolled Keywords: dmsp synthesis,marine sulfur cycling,s-methyltarnsferases,sdg 13 - climate action,sdg 14 - life below water ,/dk/atira/pure/sustainabledevelopmentgoals/climate_action
Faculty \ School: Faculty of Science > School of Chemistry
Faculty of Science > School of Biological Sciences
Depositing User: LivePure Connector
Date Deposited: 24 May 2022 16:00
Last Modified: 04 Jul 2022 15:30
URI: https://ueaeprints.uea.ac.uk/id/eprint/85139
DOI: 10.1002/mlf2.12030

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