Alternative dimethylsulfoniopropionate biosynthesis enzymes in diverse and abundant microorganisms

Jinyan Wang, Andrew R. J. Curson, Shun Zhou, Ornella Carrión, Ji Liu, Ana R. Vieira, Keanu S. Walsham, Serena Monaco, Chun-Yang Li, Qing-Yu Dong, Yu Wang, Peter Paolo L. Rivera, Xiao-Di Wang, Min Zhang, Libby Hanwell, Matthew Wallace, Xiao-Yu Zhu, Pedro N. Leão, David J. Lea-Smith, Yu-Zhong ZhangXiao-Hua Zhang, Jonathan D. Todd

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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.

Original languageEnglish
Pages (from-to)1979–1992
Number of pages14
JournalNature Microbiology
Volume9
Issue number8
Early online date11 Jun 2024
DOIs
Publication statusPublished - Aug 2024

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