Reduction of dimethylsulfoxide to dimethylsulfide by marine phytoplankton

Abstract

Dimethylsulfoxide (DMSO) is an abundant but poorly understood methylated sulfur compound in the marine environment. One potentially significant loss pathway for DMSO is through its biological reduction to dimethylsulfide (DMS), which has been documented in a number of organisms, most notably bacteria. Here we present the first detailed study of DMSO reduction by several marine phytoplankton in axenic cultures. Reduction of DMSO was observed in four algal classes, with in vivo reduction rates ranging from 0.006 to 1.5 mmol [L cell volume] 21 s 21 at 1.0 mmol L 21 DMSO. Corresponding turnover times for measured intracellular DMSO pools varied from hours to days. Michaelis-Menton kinetic parameters were estimated for Isochrysis galbana, Thalassiosira pseudonana, and Amphidinium carterae. The half-saturation constant (K m ) and maximal rate (V max ) for DMSO reduction ranged between 0.96 and 2.7 mmol [L cell volume] 21 and 17-118 nmol [L cell volume] 21 s 21 , respectively. Our results suggest that DMSO reduction is a universal activity in marine phytoplankton, even in algae with no detectable dimethylsulfoniopropionate (DMSP). Although reduction of DMSO by marine eukaryotes may not contribute significantly to removal of DMSO from the dissolved phase, this reduction is likely to be a major source of DMS in species lacking detectable DMSP lyase activity. The ability of marine phytoplankton to reduce DMSO to DMS should allow algae to cycle these compounds as part of an antioxidant system.

Increased intracellular concentrations of DMSP and DMSO in iron‐limited oceanic phytoplankton Thalassiosira oceanica and Trichodesmium erythraeum

“…The differences in the changes in DMSP p : DMSO p ratios under nutrient limitation of growth rate in the two species may be linked to differences in the activities of DMSP cleavage enzymes and DMSO reductase enzymes. A. carterae had an orderof-magnitude-lower DMSO reductase activity than T. oceanica (Spiese et al 2009), which should greatly lower DMSO loss rates via its conversion to DMS and subsequent flux out of the cells. Moreover, unlike T. oceanica, A. carterae contains enzymes that cleave DMSP into DMS (Caruana et al 2012), providing an additional potentially large source of DMSO under oxidative stress conditions via DMS oxidation by OH radicals (or other ROS).…”

“…To the contrary, DMSO is enzymatically reduced to DMS in T. oceanica and other algae, which can create a catalytic cycle between DMSO and DMS that efficiently removes OH radicals (Spiese et al 2009). Since the more lipophilic DMS should diffuse more freely across cell membranes than the more polar DMSO, the cycling between DMSO and DMS should cause a net loss of DMSO from the cell (via its conversion to DMS), which could increase DMSP p : DMSO p ratios.…”

“…A significant increase in the intracellular concentration of DMSO under Fe limitation may also be important for the DMS cycle because of the potential importance of DMS and DMSP oxidation to DMSO under increased oxidative stress (Sunda et al 2002) and the subsequent enzymatic reduction of DMSO to DMS (Spiese et al 2009). The sensitivity to Fe limitation for other species belonging to high-DMSPproducing algal groups should also be studied not only for DMSP production but also for DMS and DMSO release and the activities of DMS-producing and DMSO-reducing enzymes.…”

“…DMSO can be produced intracellularly by marine phytoplankton (Simo et al 1998;Hatton and Wilson 2007) from the oxidation of DMSP or DMS (Sunda et al 2002). It can be enzymatically reduced back to DMS, possibly fueling a coupled DMS and DMSO antioxidant cycle (Spiese et al 2009). Under increased oxidative stress, phytoplankton may thus increase DMSO and DMS production (Spiese et al 2009).…”

“…It can be enzymatically reduced back to DMS, possibly fueling a coupled DMS and DMSO antioxidant cycle (Spiese et al 2009). Under increased oxidative stress, phytoplankton may thus increase DMSO and DMS production (Spiese et al 2009). In the Peruvian upwelling region, Riseman and DiTullio (2004) found that DMSP and DMSO correlated well with the antioxidant bcarotene.…”