Function and wide distribution of DMSOP cleaving enzymes in marine organisms

Abstract

Dimethylsulfoxonium propionate (DMSOP) is a recently identified and abundant marine organosulfur compound with purported roles in oxidative stress protection, global carbon and sulfur cycling1. Diverse algae and bacteria synthesise DMSOP from dimethylsulfoniopropionate (DMSP), which potentially limits the production of climate-active gases e.g., dimethylsulfide (DMS) generated from microbial DMSP cleavage1. Here, DMSOP was found at mM levels in saltmarsh sediment, >10-fold higher than DMSP, and orders of magnitude higher than DMSOP levels previously reported in seawater1. Moreover, we showed bacteria could utilise DMSOP as an osmoprotectant. Some bacteria also cleave DMSOP liberating dimethyl sulfoxide (DMSO), an ubiquitous marine metabolite and acrylate1, but the enzymes responsible and their environmental importance were unknown. Here, we elucidated the DMSOP cleavage mechanism/s in diverse heterotrophic bacteria, e.g., SAR11 clade and Roseobacters, and fungi and phototrophic algae, e.g., Emiliania huxleyi, not previously known to have this activity. All these diverse organisms utilised their DMSP lyase ‘Ddd’ or ‘Alma1’ enzymes, that span five protein families, to cleave DMSOP with similar specific activities to DMSP. Bacteria with DMSP lyases that used DMSP as a carbon source likewise used DMSOP. Furthermore, ddd gene transcription in these bacteria was induced by DMSOP, including dddK in SAR11 strain HTCC1062. We determined the structure of DddK bound to DMSOP and concluded that the catalytic mechanisms of DMSOP cleavage by Ddd enzymes were like those for DMSP. Given the predicted teragram DMSOP production budget1, its newly found abundance in marine sediments, and the abundance of microbial DMSP lyase genes and transcripts in marine environments, DMSOP cleavage is likely a globally significant process influencing global carbon and sulfur fluxes and marine ecological interactions.

Diel variation of seawater volatile organic compounds, DMSP-related compounds, and microbial plankton inside and outside a tropical coral reef ecosystem

“…We note that DMSO can also be produced through cleavage of the recentlydiscovered intracellular component DMSOP (Thume et al, 2018), which unfortunately was not measured. A variety of microorganisms, including the microalgae haptophytes and dinoflagellates and the bacteria SAR11 and Rhodobacteriales, are capable of cleaving DMSOP to DMSO and acrylate using the same lyases for DMSP (Carrioń et al, 2023).…”

Novel dimethylsulfoniopropionate biosynthesis enzymes in diverse marine bacteria, cyanobacteria and abundant algae

“…Assuming that the known S-methyltransferase genes in microbial DMSP synthesis pathways were the major isoforms, which our analysis of algal transcriptomes implied they were, it was puzzling as to why these genes and their transcripts were not more abundant in marine systems. This is an especially relevant question considering the ubiquity of DMSP and DMSP [57] catabolic genes/transcripts, e.g., dddP, predicted to be in 17.5% and 2.0% of SRF marine bacteria, respectively [64] . There are still many DMSP-producers that lack known DMSP synthesis genes, e.g., DMSP-producing plants, macroalgae such as Ulva spp., cyanobacteria such as Trichodesmium and Synechococcus [64] , and other bacteria, like Marinobacter sp.…”

“…This is an especially relevant question considering the ubiquity of DMSP and DMSP [57] catabolic genes/transcripts, e.g., dddP, predicted to be in 17.5% and 2.0% of SRF marine bacteria, respectively [64] . There are still many DMSP-producers that lack known DMSP synthesis genes, e.g., DMSP-producing plants, macroalgae such as Ulva spp., cyanobacteria such as Trichodesmium and Synechococcus [64] , and other bacteria, like Marinobacter sp. [8] , but these are not expected to be major DMSP producers on the same scale as Haptophyta and Dinophyta algae for example.…”