Identification of a membrane transporter for dimethylsulfoniopropionate uptake in marine eukaryotic phytoplankton

Abstract

Marine microalgae obtain essential sulfur through energetically costly, assimilatory reduction of sea-salt sulfate, so the ability for osmotrophic incorporation of reduced sulfur would confer them adaptability in energy-limiting conditions. Dimethylsulfoniopropionate (DMSP) is a common marine osmolyte whose pervasive occurrence in seawater makes it as good a candidate for supplying reduced sulfur to marine eukaryotes as it is to prokaryotes. Despite earlier recognition of DMSP uptake by some phytoplankters, the mechanism and its taxonomic and geographic distributions have remained unknown. Here we show that DMSP uptake occurs in taxonomically diverse eukaryotic phytoplankton harbouring PaDT (for picoalgal DMSP transporter), a gene within the betaine/choline/carnitine transporter (BCCT) family whose transcription was upregulated by DMSP additions. Confirmation that PaDT encodes a functional DMSP transporter was obtained by restoring DMSP uptake in a BCCT-deficient mutant of Escherichia coli complemented with picoalgal PaDT. Increase of picoalgal DMSP uptake and PaDT transcription under decreasing light supports exogenous DMSP incorporation as an energy-saving strategy. The global and taxonomic spread of PaDT expression in the surface ocean indicates that eukaryotic phytoplankton are not only the main DMSP source but also a ubiquitous sink, reinforcing their role in regulating marine sulfur emissions. In this study, the authors show that marine eukaryotic phytoplankton widely take up the sulfur compound DMSP via the BCCT family transporter PaDT, suggesting an energy-saving strategy in some taxa and a dual role for phytoplankton as both a source and a sink in organosulfur cycling.