Identification of G protein-coupled receptor signaling pathway proteins in marine diatoms using comparative genomics

Abstract

BackgroundThe G protein-coupled receptor (GPCR) signaling pathway plays an essential role in signal transmission and response to external stimuli in mammalian cells. Protein components of this pathway have been characterized in plants and simpler eukaryotes such as yeast, but their presence and role in unicellular photosynthetic eukaryotes have not been determined. We use a comparative genomics approach using whole genome sequences and gene expression libraries of four diatoms (Pseudo-nitzschia multiseries, Thalassiosira pseudonana, Phaeodactylum tricornutum and Fragilariopsis cylindrus) to search for evidence of GPCR signaling pathway proteins that share sequence conservation to known GPCR pathway proteins.ResultsThe majority of the core components of GPCR signaling were well conserved in all four diatoms, with protein sequence similarity to GPCRs, human G protein α- and β-subunits and downstream effectors. There was evidence for the Gγ-subunit and thus a full heterotrimeric G protein only in T. pseudonana. Phylogenetic analysis of putative diatom GPCRs indicated similarity but deep divergence to the class C GPCRs, with branches basal to the GABAB receptor subfamily. The extracellular and intracellular regions of these putative diatom GPCR sequences exhibited large variation in sequence length, and seven of these sequences contained the necessary ligand binding domain for class C GPCR activation. Transcriptional data indicated that a number of the putative GPCR sequences are expressed in diatoms under various stress conditions in culture, and that many of the GPCR-activated signaling proteins, including the G protein, are also expressed.ConclusionsThe presence of sequences in all four diatoms that code for the proteins required for a functional mammalian GPCR pathway highlights the highly conserved nature of this pathway and suggests a complex signaling machinery related to environmental perception and response in these unicellular organisms. The lack of evidence for some GPCR pathway proteins in one or more of the diatoms, such as the Gγ-subunit, may be due to differences in genome completeness and genome coverage for the four diatoms. The high divergence of putative diatom GPCR sequences to known class C GPCRs suggests these sequences may represent another, potentially ancestral, subfamily of class C GPCRs.

Finding a partner in the ocean: molecular and evolutionary bases of the response to sexual cues in a planktonic diatom

“…In the RNA‐seq data, PSNMU‐V1.4_AUG‐EV‐PASAV3_0072880.1, homologous to GPCR3 (Port et al ., 2013), is upregulated, and the inositol phospholipid signalling pathway, which is downstream of GPCRs, also appears to be employed by P. multistriata cells to transduce information (Table S10). GPCRs bind many signalling molecules and our data indicate that they might be involved in the perception of mating cues in diatoms, as has been reported in yeast (Alvaro & Thorner, 2016).…”

Profiling of the Early Nitrogen Stress Response in the Diatom Phaeodactylum tricornutum Reveals a Novel Family of RING-Domain Transcription Factors

“…Besides P. tricornutum, two other diatoms also have fully assembled and publicly available genome sequences, namely T. pseudonana (Armbrust et al, 2004) and F. cylindrus (Port et al, 2013). These two species contain four and three RGQ-like proteins, respectively.…”

“…To date, several diatom genomes have been sequenced, among which two are considered model species, the centricate Thalassiosira pseudonana and the pennate Phaeodactylum tricornutum (Armbrust et al, 2004;Bowler et al, 2008). Other currently sequenced diatom genomes include Fragilariopsis cylindrus and Pseudo-nitzschia multiseries (Port et al, 2013) and Thalassiosira oceanica (Lommer et al, 2012); however, the latter two have not been fully assembled yet. The analysis of these genomes showed that there is a large fraction of diatom-specific genes, that diatoms have acquired genes from a variety of other organisms through horizontal gene transfer, and that often relatively little overlap exists between diatom species (Bowler et al, 2008).…”

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

“…Although the importance of GPCR signaling has been repeatedly demonstrated in multicellular eukaryotes, there is much to be discovered in unicellular eukaryotes. Components of GPCR signaling pathways have been identified in the genomes of only four diatoms— Pseudo‐nitzschia multiseries , Thalassiosira pseudonana , Phaeodactylum tricornutum , and Fragilariopsis cylindrus (Port et al )—and the prevalence of GPCR signaling has not yet been examined among dinoflagellates. Moreover, a comprehensive overview of diatom GPCR signaling pathway components and their relationships with the versions found in dinoflagellates is lacking.…”