Abstract

BackgroundG protein-coupled receptors (GPCRs) play a central role in eukaryotic signal transduction. However, the GPCR component of this signalling system, at the early origins of metazoans is not fully understood. Here we aim to identify and classify GPCRs in Amphimedon queenslandica (sponge), a member of an earliest diverging metazoan lineage (Porifera). Furthermore, phylogenetic comparisons of sponge GPCRs with eumetazoan and bilaterian GPCRs will be essential to our understanding of the GPCR system at the roots of metazoan evolution.ResultsWe present a curated list of 220 GPCRs in the sponge genome after excluding incomplete sequences and false positives from our initial dataset of 282 predicted GPCR sequences obtained using Pfam search. Phylogenetic analysis reveals that the sponge genome contains members belonging to four of the five major GRAFS families including Glutamate (33), Rhodopsin (126), Adhesion (40) and Frizzled (3). Interestingly, the sponge Rhodopsin family sequences lack orthologous relationships with those found in eumetazoan and bilaterian lineages, since they clustered separately to form sponge specific groups in the phylogenetic analysis. This suggests that sponge Rhodopsins diverged considerably from that found in other basal metazoans. A few sponge Adhesions clustered basal to Adhesion subfamilies commonly found in most vertebrates, suggesting some Adhesion subfamilies may have diverged prior to the emergence of Bilateria. Furthermore, at least eight of the sponge Adhesion members have a hormone binding motif (HRM domain) in their N-termini, although hormones have yet to be identified in sponges. We also phylogenetically clarified that sponge has homologs of metabotropic glutamate (mGluRs) and GABA receptors.ConclusionOur phylogenetic comparisons of sponge GPCRs with other metazoan genomes suggest that sponge contains a significantly diversified set of GPCRs. This is evident at the family/subfamily level comparisons for most GPCR families, in particular for the Rhodopsin family of GPCRs. In summary, this study provides a framework to perform future experimental and comparative studies to further verify and understand the roles of GPCRs that predates the divergence of bilaterian and eumetazoan lineages.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-014-0270-4) contains supplementary material, which is available to authorized users.

Highlights

  • G protein-coupled receptors (GPCRs) play a central role in eukaryotic signal transduction

  • In order to better understand the components of the GPCR system and its evolution at the early origins of Metazoa, we aimed to curate a complete set of GPCRs in sponge, as well as provide a comparative analysis with GPCRs found in eumetazoans (Nematostella and Trichoplax) and bilaterians

  • Identification and classification of GPCRs in sponge In order to generate a complete set of sponge GPCRs, we aligned the sponge proteome with Hidden Markov Models (HMM) of the 14831 families contained within the Protein families database (Pfam) database

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Summary

Introduction

G protein-coupled receptors (GPCRs) play a central role in eukaryotic signal transduction. Only a few homologues of the Rhodopsin family were found in basal fungi and Rhodopsin GPCRs were not found in choanoflagellates (Monosiga brevicollis and Salpingoeca rosetta) and filasterean Capsaspora owczarzaki [9,10] These closest metazoan relatives are limited to only a few genes coding for Adhesion and Glutamate GPCR families. Additional studies on some specific subsets of sponge GPCRs such as Glutamate [13] and Frizzled [14] provided further insights into the GPCR component in sponge Taken together this suggests that the last common ancestor of metazoans possessed a complex GPCR system, perhaps with expansions within the Rhodopsin family in comparison to pre-metazoan lineages like Choanoflagellata [15] and Filasterea [16]. Previous mining of GPCRs in a cnidarian, Nematostella vectensis and a placozoan, Trichoplax adhaerens revealed that these pre-bilaterian metazoans contained a large GPCR repertoire with 890 and 420 GPCR coding genes, respectively [17,18]

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