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.

Keywords: DMSP; Roseobacter; dimethylsulfoniopropionate; evolution; phytoplankton.

FIGURE 1

Proposed DMSP biosynthetic pathways. Structures in brackets have been detected and verified. Complete arrows signify reactions that are identified or predicted based on the observed intermediates. Dotted arrows signify unknown reactions. 1, aminotransferase; 2, NADPH-reductase; 3, methyltransferase; 4, decarboxylase; 5, oxidase; 6, decarboxylase/transaminase; 7, dehydrogenase. MTOB, 4-methylthio-2-oxobutyrate; MTHB, 4-methylthio-2-hydroxybutyrate; DMSHB, 4-dimethylsulfonio-2-hydroxybutyrate; SMM, S-methyl-L-methionine. (Hanson et al., 1994; James et al., 1995; Kocsis et al., 1998; Summers et al., 1998; Kocsis and Hanson, 2000; Lyon et al., 2011; Raina et al., 2013).

FIGURE 2

Bacterial DMSP demethylation and cleavage pathways. The DMSP demethylation pathway is catalyzed by the DMSP demethylase (DmdA), MMPA-CoA ligase (DmdB), MMPA-CoA dehydrogenase (DmdC), and either the MTA-CoA hydratase (DmdD) or acrylate utilization hydratase (AcuH). The cleavage pathway is catalyzed by a DMSP lyase (DddP, DddW, DddY, DddQ, DddL, DddK, or the algal Alma1), an acrylate-CoA ligase (PrpE), and an acryloyl-CoA reductase (AcuI). AcuH catalyzes a side reaction forming 3-hydroxypropionyl-CoA in the cleavage pathway. Revised from Reisch et al. (2011b, 2013).

FIGURE 3

Phylogenetic species tree representing the diversity of organisms that possess enzymes from the DMSP demethylation pathway and the DMSP lyases. The relatedness of representative lineages is indicated schematically on the left. Colored filled circles represent the presence of the indicated protein-encoding gene. Protein designations and query sequences are as follows: From R. pomeroyi, DmdA (SPO1913); DmdB1 (SPO0677); DmdB2 (SPO2045); DmdC1 (SPO3805); DmdC2 (SPO0298); DmdC3 (SPO2915); DmdD (SPO3804); and AcuH (SL1157_0807) from R. lacuscaerulensis. DMSP lyase protein designations and query sequences are R. pomeroyi DddP (SPO2299), DddW (SPO0453), DddQ (SPO1596), DddD (SPO1703); A. faecalis DddY (ADT64689.1); R. sphaeroides DddL (RSP1433), P. ubique DddK (SAR11_0394); E. huxleyi Alma1 (XP_005784450). The e value cut off used in all cases was < e 10^-70 with the exception of DddW (cut off of < e 10^-40) and DddQ (cut off of < e 10^-30). See Figure 2 for the names of the enzymes.

FIGURE 4

Structural similarity of the glycine cleavage T-protein and the DMSP demethylase (DmdA). Crystal structures of the (A) glycine cleavage T-protein from Thermotoga maritima (Lee et al., 2004) (PBD ID:1WOO) and (B) the DmdA monomer from P. ubique (Schuller et al., 2012) showing the shared tri-domain structure.

FIGURE 5

Structural similarities of the MTA-CoA hydratase and the enoyl-CoA hydratase from rat liver. Comparison of the structures of the R. pomeroyi MTA-CoA hydratase (DmdD, E121A mutant) monomer (cyan) in complex with MTA-CoA (green) and the rat liver ECH monomer (gray) in complex with acetoacetyl-CoA (gray) (Engel et al., 1996). The red arrow indicates a difference in the conformation of the C-terminal loop between the two structures. Figure reproduced from Tan et al. (2013).