Dimethylsulfoniopropionate: Its Sources, Role in the Marine Food Web, and Biological Degradation to Dimethylsulfide

Abstract

The massive quantities of phytoplankton in the North Atlantic and Antarctic oceans producing dimethylsulfoniopropionate (DMSP) as an osmoprotectant, much of which is degraded by marine bacteria to dimethylsulfide (DMS), ensures an important role for both compounds in the global sulfur cycle. The closest to a comprehensive review on this topic is a book of symposium proceedings edited by Kiene et al. (75); the more recent developments related specifically to DMSP degradation by microbial communities are found elsewhere (68). This article is more comprehensive, as it includes some of the earlier literature in describing the sources of DMSP, its release and linkage to the marine (primarily microbial) food web and subsequent degradation via cleavage to DMS and acrylic acid or demethylation and demethiolation to methanethiol.DMS production from DMSP has long been associated with marine algae according to the following reaction (20, 22):DMSP is a tertiary sulfonium compound produced in high concentration by certain species of marine algae and plant halophytes for the regulation of their internal osmotic environment (1,41,47,120), although its role in plants remains unclear. This alga-associated, i.e., particulate DMSP (DMSPp), when released into the marine environment as dissolved DMSP (DMSPd), can serve as a link between primary production and the microbial population, as it is readily degraded by chemoheterotrophic bacteria (59). DMSP turnover usually exceeds DMS production in natural waters (60) because DMSP is also demethylated to 3-methiolpropionate, which can be further demethylated to 3-mercaptopropionate or demethiolated, releasing methanethiol (72,118). These reactions will be discussed in more detail below.The biogeochemical significance of DMSP cleavage was first suggested in 1972, when DMS was found to be universally present in seawater and emitted at a significant rate to the atmosphere (87). It was proposed that DMS, rather than H 2 S from coastal waters and mud flats, was the missing gaseous sulfur compound needed to enable the steady-state flow of sulfur between marine and terrestrial environments, making DMS emissions a key step in the global sulfur cycle (87). Atmospheric H 2 S, which arises primarily from dissimilatory sulfate reduction in organic matter-rich environments, could never be measured in sufficient quantity to be the vehicle for transferring large quantities of sulfur from sea to air to land.The total annual flux of biogenic DMS released to the atmosphere ranges from 28 to 45 Tg of S year Ϫ1 , at least 10-fold higher than from all other sources (Table 1). Recent, more comprehensive calculations of global annual DMS flux from the oceans gave values that ranged from 13 to 37 Tg of S year Ϫ1 (57). This sea-to-air flux represents about 50% of the global biogenic sulfur flux to the atmosphere (3). However, anthropogenic sulfur emissions dominate the sulfur flux, representing 80 to 90% of the input to the global sulfur cycle (12,23,88).The magnitude of the marine DMS emissions is all the more ...

Dimethylsulfoniopropionate, superoxide dismutase and glutathione as stress response indicators in three corals under short-term hyposalinity stress

“…An increase in host caspase 3-like activity (a measure of the initiation of a cell death response) was however recorded in P. damicornis at the lowest salinity (H (2) ¼ 8.867, p ¼ 0.01, electronic supplementary material, figure S1i). Freshwater dilutions resulted in altered seawater carbonate chemistry, with a significant decrease in total alkalinity (H (2) figure 2a; dark grey bars), whereas no statistical difference or change was detected in S. pistillata or P. damicornis (figure 2b,c). Host glutathione (GS x ) increased with decreasing salinity in all three species (A. millepora H (2) ¼ 11.17, p ¼ ,0.001, figure 3a; light grey bars, S. pistillata H (2) ¼ 10.67, p ¼ ,0.001, figure 3b and figure 3c).…”

“…Dimethylsulfoniopropionate (DMSP) represents a major fraction of organic sulfur within marine systems [1,2] and is produced by many macroalgae and microalgal species, including dinoflagellates from the genus Symbiodinium. Scleractinian or reef-building corals, which comprise a symbiosis between an animal host (Cnidarian phylum) and a symbiotic dinoflagellate algae (Symbiodinium), are among the largest producers of DMSP [3,4].…”

Transcriptomic analysis of a marine bacterial community enriched with dimethylsulfoniopropionate

“…Both the DMSP demethylation and cleavage pathways yield a C3 compound, possibly acrylate (Kiene and Linn, 2000b), although recent studies suggest that acryloyl-CoA or 3-OH-propionate can also be intermediates (Curson et al, 2008;Todd et al, 2010). Studies of marine and freshwater isolates have shown that some bacteria can grow on acrylate by conversion to 3-OH-propionate (Kiene, 1990;Ansede et al, 1999Ansede et al, , 2001Yoch, 2002). The pattern of transcript enrichment after DMSP addition suggests that the most common degradation pathway of the C3 moiety of DMSP is to acetyl-CoA by malonyl-CoA (Figure 2, see abundances of propanoate-related transcripts in Supplementary Table S5), although this is likely to be taxon-dependent and possibly temporally variable.…”

“…Alternatively, DMSP can be cleaved to produce DMS and a C3 compound (Kiene and Linn, 2000b;Todd et al, 2007). Cultured bacteria that are able to carry out both pathways have been described Yoch, 2002), and assimilation of the sulfur moiety appears to be a widespread capability in natural bacterial communities (Yoch, 2002;Malmstrom et al, 2004a;Vila-Costa et al, 2007). However, for most bacterial transformations involved in DMSP degradation, the identity of the main bacterial groups, and the factors controlling the biological switch between DMSP pathways, remain poorly understood.…”

The opportunistic coral pathogen Aspergillus sydowii contains dddP and makes dimethyl sulfide from dimethylsulfoniopropionate

“…When released from such organisms, other marine microbes can use several wholly different ways to catabolize DMSP (Yoch, 2002;Johnston et al, 2007;Howard et al, 2008). Worldwide, these biotransformations annually turn over B10 9 tons of DMSP.…”