Dimethyl sulfide acts as eat-me signal during microbial predator-prey interactions in the ocean

Abstract Phytoplankton are key components of the oceanic carbon and sulfur cycles 1. During bloom events, some species can emit massive amounts of the organosulfur volatile dimethyl sulfide (DMS) to the atmosphere, where it can modulate aerosol formation and affect climate. In aquatic environments, DMS plays an important role as a chemical signal mediating diverse trophic-level interactions. Yet its role in microbial predator-prey interactions remains elusive with contradicting evidence for its role in algal chemical defense and in grazer’s chemoattraction to prey cells. Here, we investigated the signaling role of DMS during zooplankton-algae interactions by genetic and biochemical manipulation of the algal DMS-generating enzyme (Dimethylsulfoniopropionate lyase, DL) from the bloom-forming alga Emiliania huxleyi. We inhibited DL activity in live E. huxleyi cells by the novel DL-inhibitor 2-bromo-3-(dimethylsulfonio)-propionate (Br-DMSP) , and overexpressed DL in the model diatom Thalassiosira pseudonana. We showed that algal DL activity did not serve as anti-grazing chemical defense, and paradoxically enhanced grazing by the model microzooplankton Oxyrrhis marina and other micro- and mesozooplankton, including ciliates and copepods. Consumption of algal prey with induced DL activity also promoted O. marina’s growth. Overall, our results demonstrate that DMS-mediated herbivory may be ecologically important and prevalent during prey-predator dynamics in oceanic ecosystems. The role of DMS as an appetizing signal to grazers revealed here raises fundamental questions regarding the retention of its biosynthetic enzyme through the evolution of dominant bloom-forming phytoplankton in the ocean.