A steady-state physiological model for intracellular dimethylsulfoxide in marine phytoplankton

Abstract

Environmental context Dimethylsulfoxide (DMSO) is important in the biogeochemical cycle of sulfur. Using a mathematical flux model of DMSO production and loss rates, we find that the high intracellular DMSO concentrations measured in phytoplankton cannot be produced without invoking unrealistically high intracellular concentrations of the precursor dimethylsulfoniopropionate, or much lower phytoplankton cellular efflux rates than currently reported. Our study emphasises the need for further investigations of DMSO fluxes across intracellular and outer cell membranes. Abstract Despite 20+ years of research, the mechanisms whereby marine phytoplankton accumulate high dimethylsulfoxide (DMSO) concentrations (up to 1–70mmol per litre of cell volume) are still puzzling. In order to evaluate reported intracellular DMSO concentrations, we constructed a kinetic steady-state rate model of intracellular DMSO concentrations in microalgae based on reported DMSO production from the oxidation of dimethylsulfoniopropionate (DMSP) and loss by diffusion out of the cell. Based on measured rates of DMSO diffusion across the outer cell membrane of model algal species, the steady-state model indicates that sustaining intracellular DMSO concentrations in the millimolar range by the oxidation of intracellular DMSP would require steady-state intracellular DMSP concentrations that are 40 to 10000 times higher than values measured in prymnesiophytes and diatoms, high- and low-DMSP algal groups. However, if DMSO is mainly produced within the chloroplast by the oxidation of DMSP by photosynthetically produced reactive oxygen species, it would have to diffuse through multiple chloroplast membranes before being lost from the cell across the outer membrane. Consequently, its loss rate might be considerably slower than our model predicts, allowing the build-up of higher intracellular DMSO concentrations. Possible biases in sample handling and DMSO analyses could also explain the discrepancy between modelled and measured intracellular DMSO.