A new route for synthesis of dimethylsulphoniopropionate in marine algae

Abstract

The 3-dimethylsulphoniopropionate (DMSP) produced by marine algae is the main biogenic precursor of atmospheric dimethylsulphide (DMS). This biogenic DMS, formed by bacterial and algal degradation of DMSP, contributes about 1.5 x 10(13) g of sulphur to the atmosphere annually, and plays a major part in the global sulphur cycle, in cloud formation and potentially in climate regulation. Although DMSP biosynthesis has been partially elucidated in a higher plant, nothing is known about how algae make DMSP except that the whole molecule is derived from methionine. Here we use in vivo isotope labelling to demonstrate that DMSP synthesis in the green macroalga Enteromorpha intestinalis proceeds by a route entirely distinct from that in higher plants. From methionine, the steps are transamination, reduction and S-methylation to give the novel sulphonium compound 4-dimethylsulphonio-2-hydroxybutyrate (DMSHB), which is oxidatively decarboxylated to DMSP. The key intermediate DMSHB was also identified in three diverse phytoplankton species, indicating that the same pathway operates in other algal classes that are important sources of DMS. The fact that a transamination initiates this pathway could help explain how algal DMSP (and thereby DMS) production is enhanced by nitrogen deficiency.

The Response of Diatom Central Carbon Metabolism to Nitrogen Starvation Is Different from That of Green Algae and Higher Plants

“…Keller et al (1999) also found that DMSP increased in T. pseudonana under nitrogen-limited conditions, while the nitrogenous osmolytes, including Gly betaine and amino acids, were depleted. The proteins involved in the DMSP biosynthesis pathway have yet to be identified, although it is thought that the first step involves the transamination of Met, to yield the 2-oxo acid 4-methylthio-2-oxobutyrate (Gage et al, 1997). As discussed above, we identified a branched-chain aminotransferase (ProtID 260934) as the most highly increased protein at the onset of nitrogen starvation, and this may be a candidate for the enzyme catalyzing this step.…”

Proteomic Analysis of a Sea-Ice Diatom: Salinity Acclimation Provides New Insight into the Dimethylsulfoniopropionate Production Pathway

“…conversion of Met to DMSP based on radiolabeling metabolite studies (Gage et al, 1997;Summers et al, 1998) would be elevated in association with salinityinduced DMSP elevation. Eighteen of the 36 proteins increased under high-salinity/DMSP conditions classified within the four enzyme classes in the proposed Met-DMSP synthesis pathway (Fig.…”

“…Microalgae, such as sea-ice diatoms, are believed to utilize an alternative Met transaminase pathway. Radiolabeling studies of pathway metabolites showed algal DMSP synthesis sequentially utilizes 2-oxoglutarate-dependent aminotransferase, NADPH-linked reductase, S-adenosyl Met (SAM)-dependent methyltransferase (SAMmt), and oxidative decarboxylase (Gage et al, 1997;Summers et al, 1998). Analyzed most extensively in the green macroalgae, Ulva intestinalis, radiolabeled metabolites also supports presence of this pathway in haptophyte, diatom, and prasinophyte species.…”

“…According to the proposed algal DMSP synthesis pathway (Gage et al, 1997;Fig. 6), the first step to convert Met to DMSP is catalyzed by an oxoglutaratedependent AT, creating the intermediate metabolite 4-methylthio-2-oxobutyrate.…”

“…In an attempt to be more representative of natural salinity change, salinity was gradually manipulated over a 22-h period, and both pH and carbonate alkalinity were allowed to covary with salinity, as occurs within sea ice (Papadimitriou et al, 2007). We hypothesized that proteins associated with Met synthesis and from enzyme classes that drive reactions described in DMSP metabolite radiolabeling studies (Gage et al, 1997;Summers et al, 1998) will increase in abundance during hypersaline-induced DMSP accumulation. Identification of candidate proteins that may regulate DMSP synthesis will enable targeted studies on biological controls of DMSP production, which in turn can lead to improved modeling of environmental and biological feedbacks on potential DMS climate effects.…”