Phytoplankton are key components of the oceanic carbon and sulfur cycles1. During bloom events, some species can emit large amounts of the organosulfur volatile dimethyl sulfide (DMS) into the ocean and consequently the atmosphere, where it can modulate aerosol formation and affect climate2,3. In aquatic environments, DMS plays an important role as a chemical signal mediating diverse trophic interactions. Yet, its role in microbial predator–prey interactions remains elusive with contradicting evidence for its role in either algal chemical defence or in the chemo-attraction of grazers to prey cells4,5. Here we investigated the signalling role of DMS during zooplankton–algae interactions by genetic and biochemical manipulation of the algal DMS-generating enzyme dimethylsulfoniopropionate lyase (DL) in the bloom-forming alga Emiliania huxleyi6. We inhibited DL activity in E. huxleyi cells in vivo using the selective DL-inhibitor 2-bromo-3-(dimethylsulfonio)-propionate7 and overexpressed the DL-encoding gene in the model diatom Thalassiosira pseudonana. We showed that algal DL activity did not serve as an anti-grazing chemical defence but paradoxically enhanced predation by the grazer Oxyrrhis marina and other microzooplankton and mesozooplankton, including ciliates and copepods. Consumption of algal prey with induced DL activity also promoted O. marina growth. Overall, our results demonstrate that DMS-mediated grazing may be ecologically important and prevalent during prey–predator dynamics in aquatic ecosystems. The role of algal DMS revealed here, acting as an eat-me signal for grazers, raises fundamental questions regarding the retention of its biosynthetic enzyme through the evolution of dominant bloom-forming phytoplankton in the ocean.
Bibliographical noteFunding Information:
We thank I. Nussbaum and A. Spierer for assisting in laboratory experiments, Y. Finkel for helping in genetic transformation of T. pseudonana, D. Meltzer (Weizmann Institute of Science, Israel) for synthesizing Br-DMSP used in grazing experiments, E. M. Avrahami for conducting scanning electron microscopy analysis for T. pseudonana cells, Y. Avrahami for helping with field sampling and flow cytometry and C. Kuhlisch for her constructive feedback on the manuscript. We thank the Inter-University Institute for Marine Sciences in Eilat for access to its infrastructure and services. We gratefully acknowledge financial support from the Israeli Science Foundation (grant no. 1515/15 and 1972/20) and the support by a research grant from the Estate of Bernard Berkowitz both awarded to A.V. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. During the final preparation of this paper, Prof. D. S. Tawfik died tragically; he was a brilliant, world-renowned scientist with a great passion to explore protein evolution. We would like to dedicate this paper to his memory.
© 2021, The Author(s), under exclusive licence to Springer Nature Limited.