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): (1) 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 H2S 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 H2S, 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−1, at least 10-fold higher than from all other sources (Table ​(Table1).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−1 (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). TABLE 1. Estimates of natural emissions of organosulfur compoundsa The magnitude of the marine DMS emissions is all the more remarkable considering that over half of the DMSP released is demethylated (68) and that a significant fraction of the DMS is oxidized by bacteria in the water column before it can be released to the atmosphere (13, 64). While most of the biogenic sulfur emissions (primarily DMS) come from the oceans, those coming from salt marshes and coastal wetlands are many times higher on a unit area basis (112). DMS flux per unit area from these marine wetlands is also much higher than from any known terrestrial soil (2). The biogeochemical cycling of DMSP and its biological degradation products are shown in Fig. ​Fig.11. FIG. 1. Scheme representing the mechanisms of DMSP and DMS cycling in the marine water column and atmosphere. DMSO, dimethyl sulfoxide; CCN, cloud-condensing nuclei; MMPA, 3-methiolpropionate; β-HP, β-hydroxypropionate; 3-MPA, 3-mercaptopropionate; ...