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

Chun-Yang Li, Jason C. Crack, Simone Newton-Payne, Andrew R. J. Murphy, Xiu-Lan Chen, Benjamin J. Pinchbeck, Shun Zhou, Beth T. Williams, Ming Peng, Xiao-Hua Zhang, Yin Chen, Nick E. Le Brun, Jonathan D. Todd, Yu-Zhong Zhang

Research output: Contribution to journalArticlepeer-review

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.
Original languageEnglish
JournalmLife
Early online date15 Jun 2022
DOIs
Publication statusE-pub ahead of print - 15 Jun 2022

Keywords

  • DMSP synthesis
  • marine sulfur cycling
  • S-methyltarnsferases

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