Evolution of Dimethylsulfoniopropionate Metabolism in Marine Phytoplankton and Bacteria

Abstract

The elucidation of the pathways for dimethylsulfoniopropionate (DMSP) synthesis and metabolism and the ecological impact of DMSP have been studied for nearly 70 years. Much of this interest stems from the fact that DMSP metabolism produces the climatically active gas dimethyl sulfide (DMS), the primary natural source of sulfur to the atmosphere. DMSP plays many important roles for marine life, including use as an osmolyte, antioxidant, predator deterrent, and cryoprotectant for phytoplankton and as a reduced carbon and sulfur source for marine bacteria. DMSP is hypothesized to have become abundant in oceans approximately 250 million years ago with the diversification of the strong DMSP producers, the dinoflagellates. This event coincides with the first genome expansion of the Roseobacter clade, known DMSP degraders. Structural and mechanistic studies of the enzymes of the bacterial DMSP demethylation and cleavage pathways suggest that exposure to DMSP led to the recruitment of enzymes from preexisting metabolic pathways. In some cases, such as DmdA, DmdD, and DddP, these enzymes appear to have evolved to become more specific for DMSP metabolism. By contrast, many of the other enzymes, DmdB, DmdC, and the acrylate utilization hydratase AcuH, have maintained broad functionality and substrate specificities, allowing them to carry out a range of reactions within the cell. This review will cover the experimental evidence supporting the hypothesis that, as DMSP became more readily available in the marine environment, marine bacteria adapted enzymes already encoded in their genomes to utilize this new compound.

Mechanistic insight into 3‐methylmercaptopropionate metabolism and kinetical regulation of demethylation pathway in marine dimethylsulfoniopropionate‐catabolizing bacteria

“…It is noteworthy that the ITI_1157 and ISM dmdA , dmdB and dmdC genes are up‐regulated by DMSP in the same order as the reaction sequence in the DMSP demethylation pathway with time, perhaps suggesting that the product of the previous enzyme is the inducer, which needs further investigation. The transcription of acuH is not enhanced in response to DMSP in either ITI_1157 or ISM, consistent with its surrogate role of dmdD to catalyze MTA‐CoA in this demethylation pathway (Reisch et al ., ; Bullock et al ., ).…”

“…DmdB is shown to have a higher affinity to MMPA than to acrylate, propionate or isobutyrate (Table ) (Bullock et al ., ), implying the evolution of DmdB from other pathways to the demethylation pathway for DMSP catabolism. DmdC from R. pomeroyi DSS‐3 has been reported to have lower K m s to butyrl‐CoA, valeryl‐CoA and caproyl‐CoA than to MMPA‐CoA (Table ) (Bullock et al ., ), indicating that MMPA‐CoA might not be the optimal substrate of DmdC of R. pomeroyi DSS‐3. Due to MTA‐CoA were not commercially available and difficult to prepare, we could not obtain the K m value of AcuH to MTA‐CoA, which has not been reported yet.…”

“…Finaly, the MTA‐CoA hydratase DmdD catalyzes the hydration and hydrolysis of MTA‐CoA to generate acetaldehyde and methanethiol (MeSH). Some bacteria, for example, Ruegeria lacuscaerulensis ITI_1157 and Roseovarius nubinhibens ISM, lack DmdD, but fully demethylate DMSP, utilizing a DmdD ortholog, AcuH, which functions as a MTA‐CoA hydratase (Reisch et al ., ; Bullock et al ., ). Of the Dmd enzymes, the crystal structures and the catalytic mechanisms of DmdA, DmdD and AcuH have been reported (Schuller et al ., ; Tan et al ., ; Cao et al ., ).…”

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“…It can be used as an osmolyte (e.g., brackish ecosystems), antioxidant (e.g., thermal stress), predator deterrent (e.g., phytoplankton grazed by zooplankton), chemoatractor for tertiary consumers (e.g., birds and small carnivorous fish), cryoprotectant (e.g., polar algae), as a reduced carbon and sulfur source for bacteria, and by coral polyps as a signaling molecule to attract microbial communities necessary for coral health (reviewed in ref. ).…”

“…Dimethylsulfoniopropionate (DMSP) is a highly abundant and important sulfur metabolite in marine and estuarine ecosystems. It is biosynthesized by bacteria, algae, plants, and even juvenile corals lacking endosymbionts . It can be used as an osmolyte (e.g., brackish ecosystems), antioxidant (e.g., thermal stress), predator deterrent (e.g., phytoplankton grazed by zooplankton), chemoatractor for tertiary consumers (e.g., birds and small carnivorous fish), cryoprotectant (e.g., polar algae), as a reduced carbon and sulfur source for bacteria, and by coral polyps as a signaling molecule to attract microbial communities necessary for coral health (reviewed in ref.…”