DSYB catalyses the key step of dimethylsulfoniopropionate biosynthesis in many phytoplankton

Abstract

Dimethylsulfoniopropionate (DMSP) is a globally important organosulfur molecule and the major precursor for dimethyl sulfide. These compounds are important info-chemicals, key nutrients for marine microorganisms, and are involved in global sulfur cycling, atmospheric chemistry and cloud formation. DMSP production was thought to be confined to eukaryotes, but heterotrophic bacteria can also produce DMSP through the pathway used by most phytoplankton , and the DsyB enzyme catalysing the key step of this pathway in bacteria was recently identified . However, eukaryotic phytoplankton probably produce most of Earth's DMSP, yet no DMSP biosynthesis genes have been identified in any such organisms. Here we identify functional dsyB homologues, termed DSYB, in many phytoplankton and corals. DSYB is a methylthiohydroxybutryate methyltransferase enzyme localized in the chloroplasts and mitochondria of the haptophyte Prymnesium parvum, and stable isotope tracking experiments support these organelles as sites of DMSP synthesis. DSYB transcription levels increased with DMSP concentrations in different phytoplankton and were indicative of intracellular DMSP. Identification of the eukaryotic DSYB sequences, along with bacterial dsyB, provides the first molecular tools to predict the relative contributions of eukaryotes and prokaryotes to global DMSP production. Furthermore, evolutionary analysis suggests that eukaryotic DSYB originated in bacteria and was passed to eukaryotes early in their evolution.

Differential Gene Expression Supports a Resource‐Intensive, Defensive Role for Colony Production in the Bloom‐Forming Haptophyte, Phaeocystis globosa

“…While algal genes associated with DMSP biosynthesis ( DSYB , Curson et al. ) and cleavage ( Alma family genes, Alcolombri et al. ) have been identified in many algal transcriptomes, including Phaeocystis antarctica , this study is the first to identify these genes for Phaeocystis globosa .…”

“…A blastp query against curated DSYB protein sequences from Curson et al. () and Alma family protein sequences from Alcolombri et al. () identified four Phaeocystis globosa contigs as putative DSYB or Alma family genes (Table ).…”

“…We performed blastp queries with curated DSYB protein sequences (provided by Curson et al. ) and E. huxleyi and Symbiodinium Alma family protein sequences downloaded from UniProt (July 2018) against amino acid sequences translated from the Phaeocystis globosa CCMP1528 transcriptome. Expression levels of putative Phaeocystis globosa DSYB and Alma family genes were then checked in colonial and solitary culture replicates.…”

“…Since Phaeocystis is an important marine producer of DMSP and DMS—and because these molecules may be associated with colonial defense, we queried our dataset for algal genes involved in DMSP production ( DSYB , Curson et al. ) and its cleavage to DMS and acrylate ( Alma1 , Alcolombri et al. ).…”

In Vitro Reconstitution of Bacterial DMSP Biosynthesis

“…[1a] Figure 1. [10b] Angewandte Chemie Zuschriften Only the methionine S-methyltransferase MSMT (route 2 and 3), [12a] and the methylthiohydroxybutryate S-methyltransferase DsyB (route 1), [9,14] have been identified and directly linked to DMSP production. [9][10] Spartina alterniflora (saltmarsh cordgrass), [10c, 11] and the actinobacterium Streptomyces mobaraensis produce DMSP via pathway 2( 2a-c,r ed, this work).…”