Comparative transcriptomics supports the presence of G protein-coupled receptor-based signaling in unicellular marine eukaryotes

Being abundant primary producers, single-celled eukaryotic diatoms and dinoflagellates dominate marine food webs and significantly impact the ecology of the oceans. These organisms face competition and predation which have contributed to the evolution of chemical defenses and their ability to sense chemical cues. Elucidating how these chemical cues are perceived by organisms requires identification of proteins involved in relaying chemical information to cells. The functions of G protein-coupled receptor (GPCR) signaling diversified over evolutionary time in multicellular organisms, but the role that GPCR signaling plays in unicellular eukaryotes remains largely unknown. Using comparative transcriptomic analysis, we identified repertoires of GPCR signaling proteins from 81 diatom and 36 dinoflagellate transcriptomes. Diatoms and dinoflagellates express putative GPCRs that are highly diverged from known metazoan GPCRs along with well-conserved core components of GPCR signaling pathways. Unlike other eukaryotes that express multiple classes of GPCRs, diatoms and dinoflagellates were each found to express a single, major class of putative GPCRs with greatest similarity to class C and rhodopsin-like GPCRs, respectively. Furthermore, only 4.2% of the GPCR-like transcripts from dinoflagellates were predicted to be true GPCRs compared to 48% in diatoms. These results suggest that further expansion of GPCRs did not take place within each of these two major phytoplankton groups, and that dinoflagellate GPCRs are more divergent from known GPCRs than are diatom GPCRs. Our results provide additional evidence for the global existence of relatively ancestral GPCR signaling machinery in marine phytoplankton.