Alternative dimethylsulfoniopropionate biosynthesis enzymes in diverse and abundant microorganisms

Wang, Jinyan, Curson, Andrew R. J., Zhou, Shun, Carrión, Ornella, Liu, Ji, Vieira, Ana R., Walsham, Keanu S., Monaco, Serena, Li, Chun-Yang, Dong, Qing-Yu, Wang, Yu, Rivera, Peter Paolo L., Wang, Xiao-Di, Zhang, Min, Hanwell, Libby, Wallace, Matthew ORCID: https://orcid.org/0000-0002-5751-1827, Zhu, Xiao-Yu, Leão, Pedro N., Lea-Smith, David J. ORCID: https://orcid.org/0000-0003-2463-406X, Zhang, Yu-Zhong, Zhang, Xiao-Hua and Todd, Jonathan D. (2024) Alternative dimethylsulfoniopropionate biosynthesis enzymes in diverse and abundant microorganisms. Nature Microbiology, 9 (8). 1979–1992. ISSN 2058-5276

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Abstract

Dimethylsulfoniopropionate (DMSP) is an abundant marine organosulfur compound with roles in stress protection, chemotaxis, nutrient and sulfur cycling and climate regulation. Here we report the discovery of a bifunctional DMSP biosynthesis enzyme, DsyGD, in the transamination pathway of the rhizobacterium Gynuella sunshinyii and some filamentous cyanobacteria not previously known to produce DMSP. DsyGD produces DMSP through its N-terminal DsyG methylthiohydroxybutyrate S-methyltransferase and C-terminal DsyD dimethylsulfoniohydroxybutyrate decarboxylase domains. Phylogenetically distinct DsyG-like proteins, termed DSYE, with methylthiohydroxybutyrate S-methyltransferase activity were found in diverse and environmentally abundant algae, comprising a mix of low, high and previously unknown DMSP producers. Algae containing DSYE, particularly bloom-forming Pelagophyceae species, were globally more abundant DMSP producers than those with previously described DMSP synthesis genes. This work greatly increases the number and diversity of predicted DMSP-producing organisms and highlights the importance of Pelagophyceae and other DSYE-containing algae in global DMSP production and sulfur cycling.

Item Type: Article
Additional Information: Data availability statement: Accession numbers of sequences from the NCBI and MMETSP analysed in this study are listed in Table 1 and Supplementary Tables 1 and 10. Source data are provided with the paper. Funding information: The authors acknowledge Y.R. Chung from Gyeongsang National University for kindly providing the G. sunshinyii strain and Y. Zheng and J. Liu for experimental advice. We also thank G. Yang from the Ocean University of China for help with the sampling and identification of Carex scabrifolia. Axenic O. tauri was kindly provided by V. Jackson and A. Monier at the University of Exeter. This work was funded by the National Natural Science Foundation of China (92251303 and 32370118, PI (Principal Investigator): X.-H.Z.), the Marine S&T Fund of Shandong Province for Laoshan Laboratory (2022QNLM030004-3, Co-PI: X.-H.Z.), the Fundamental Research Funds for the Central Universities (202172002, PI: X.-H.Z.), the European Union’s Horizon 2020 Research and Innovation programme under grant agreement no. 952374 (PI: P.N.L.) and the Fundação para a Ciência e a Tecnologia, Portugal, through the strategic funding grant UIDP/04423/2020 and UIDB/04423/2020 (PI: P.N.L.), Biotechnology and Biological Sciences Research Council, United Kingdom (BB/X005968, PI: J.D.T.), Natural Environmental Research Council, United Kingdom (NE/P012671, NE/S001352, NE/X000990, PI: J.D.T.) and NE/X014428 with D.L.S. and the Leverhulme trust (RPG-2020-413, PI: J.D.T.). We acknowledge funding support from the BBSRC Norwich Research Park Doctoral Training Partnership programme (BB/2244848, K.S.W.) and (BB/M011216/1, L.H.), UKRI for funding via a Future Leaders Fellowship (MR/T044020/1, M.W.), the National Natural Science Foundation of China (32330001, PI: Y.-Z.Z.), Shandong Provincial Natural Science Foundation (ZR2022QD003, J.L.) and the Taishan Scholars Program of Shandong Province, China (tsqn202306092, PI: C.-Y.L.).
Uncontrolled Keywords: applied microbiology and biotechnology,microbiology (medical),genetics,cell biology,microbiology,immunology,sdg 14 - life below water,sdg 13 - climate action ,/dk/atira/pure/subjectarea/asjc/2400/2402
Faculty \ School: Faculty of Science > School of Biological Sciences
Faculty of Science
Faculty of Science > School of Chemistry, Pharmacy and Pharmacology
University of East Anglia Research Groups/Centres > Theme - ClimateUEA
UEA Research Groups: Faculty of Science > Research Groups > Pharmaceutical Materials and Soft Matter
Faculty of Science > Research Groups > Molecular Microbiology
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Depositing User: LivePure Connector
Date Deposited: 26 Apr 2024 14:31
Last Modified: 04 Dec 2024 01:41
URI: https://ueaeprints.uea.ac.uk/id/eprint/95031
DOI: 10.1038/s41564-024-01715-9

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