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

Abstract

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.

Predator cues target signaling pathways in toxic algal metabolome

“…Based on prior studies (Wohlrab et al 2010; Amato et al 2018; Li and Ismar 2018; Harðardóttir et al 2019; Mojib and Kubanek 2020), copepodamides were hypothesized to act as agonists of GPCRs, triggering a signaling cascade that results in amplified toxin production in A. minutum . However, when the GPCR inhibitor SCH‐202676 was applied to A. minutum to prevent binding of ligands to GPCRs (Fawzi et al 2001), toxin concentrations rose significantly (GPCR inhibition: F 1,32 = 9.3, p = 0.004; Supporting Information Fig.…”

“…In the diatom Skeletonema marinoi , copepod cues boosted cAMP activity (Amato et al 2018) whereas in A. tamarense cAMP was reduced (Wohlrab et al 2010). This is likely due to major differences in the structures and functions of the predominant GPCRs and G protein signaling in diatoms and dinoflagellates (Mojib and Kubanek 2020). Perhaps copepodamides interact further upstream in the pathway in diatoms.…”

“…Perhaps copepodamides interact further upstream in the pathway in diatoms. Alternatively, due to the shorter length of the N‐terminus and differences in the transmembrane domains in the more primitive dinoflagellate GPCRs (Mojib and Kubanek 2020), copepodamides may act as antagonists to dinoflagellate GPCRs and as agonists in diatoms. Consequently, further studies are warranted to tease out the mechanism by which copepodamides might interact with GPCRs and G protein signaling.…”

“…Based on upregulation of G protein‐coupled receptors (GPCRs), Zhu and colleagues suggested that these chemoreceptors are involved in green algal recognition of Daphnia grazing cues (Zhu et al 2021). GPCRs have also been identified among diatom and dinoflagellate phytoplankton taxa (Mojib and Kubanek 2020); however, their potential role in predator cue recognition has not been deeply studied. To date, only a handful of studies have pursued the signaling cascade in diatoms and dinoflagellates triggered by predatory zooplankton (Wohlrab et al 2010; Amato et al 2018; Li and Ismar 2018; Harðardóttir et al 2019).…”

Linking extreme seasonality and gene expression in arctic marine protists

“…It is not clear what is their function in microbial eukaryotes, such as dinophytes [83]. However, recently, it was suggested that they are involved in G protein-coupled receptor-based signalling in Dinophyta [84].…”