Neuropeptide evolution: Chelicerate neurohormone and neuropeptide genes may reflect one or more whole genome duplications

Highlights

• Many neuropeptide and neuropeptide GPCR genes have paralogs in Chelicerates.

• These paralogs could be due to whole genome duplications.

• CCRFamide is a novel Arthropod neuropeptide gene.

Abstract

Four genomes and two transcriptomes from six Chelicerate species were analyzed for the presence of neuropeptide and neurohormone precursors and their GPCRs. The genome from the spider Stegodyphus mimosarum yielded 87 neuropeptide precursors and 120 neuropeptide GPCRs. Many neuropeptide transcripts were also found in the transcriptomes of three other spiders, Latrodectus hesperus, Parasteatoda tepidariorum and Acanthoscurria geniculata. For the scorpion Mesobuthus martensii the numbers are 79 and 93 respectively. The very small genome of the house dust mite, Dermatophagoides farinae, on the other hand contains a much smaller number of such genes. A few new putative Arthropod neuropeptide genes were discovered. Thus, both spiders and the scorpion have an achatin gene and in spiders there are two different genes encoding myosuppressin-like peptides while spiders also have two genes encoding novel LGamides. Another finding is the presence of trissin in spiders and scorpions, while neuropeptide genes that seem to be orthologs of Lottia LFRYamide and Platynereis CCRFamide were also found. Such genes were also found in various insect species, but seem to be lacking from the Holometabola. The Chelicerate neuropeptide and neuropeptide GPCR genes often have paralogs. As the large majority of these are probably not due to local gene duplications, is plausible that they reflect the effects of one or more ancient whole genome duplications.

Introduction

Neuropeptides and neurohormones regulate and/or modulate many biological processes from basal physiological functions such as carbohydrate metabolism and water balance to cognitive functions. It is possible that they were among the first chemical messengers used by the nervous and endocrine systems to establish communication between different cells of a single organism. In the last two decades a large number of genomes have been sequenced which allow in theory to identify all the neuropeptide genes they contain. In practice, this is often more difficult as neuropeptide sequences are small and relatively variable and are usually only recognized when they either code for homologs of previously identified neuropeptides or a number of very similar peptide sequences separated by putative convertase cleavage sites. Nevertheless, it seems likely that most neuropeptide genes can be identified in a given sequenced Arthropod genome.

The large majority of neuropeptides act through G-protein coupled receptors (GPCRs) which are readily identified from genome sequences for the presence of their seven transmembrane regions that are well conserved. Thus, by analyzing simultaneously both neuropeptide and their putative receptors in its genome it is possible to get a fairly complete view of the neuropeptidome of a species. Using such methods it was previously shown that the neuropeptidomes of insects, annelids and mollusks are remarkably similar and share a large number of neuropeptide genes (Veenstra, 2010, Veenstra, 2011, Stewart et al., 2014).

As expected, neuropeptides and their GPCRs identified from the spider mite Tetranychus urticae, the first Chelicerate for which a complete genome was sequenced (Grbić et al., 2011), are most similar to those of insects (Veenstra et al., 2012). However, some of its neuropeptide genes were previously only known from mollusks. One of these, elevenin, has subsequently also been found in insects (Tanaka et al., 2014, Veenstra, 2014). Since then draft genomes have been published for four other Chelicerates, those of the African social velvet spider, Stegodyphus mimosarum, the Brazilian white-knee tarantula, Acanthoscurria geniculata (Sanggaard et al., 2014), the scorpion Mesobuthus martensii (Cao et al., 2013), and the house dust mite Dermatophagoides farinae (Chan et al., 2015). At the same time spider transcriptomes have become available for Latrodectus hesperus and Parasteatoda tepidariorum (Clarke et al., 2014, Posnien et al., 2014). It thus seemed interesting to take another look at Chelicerate neuropeptides to complete the picture of Arthropod neuropeptides and their evolution. Christie (2015) has already published a number of spider neuropeptide precursors based on the Latrodectus transcriptome, but, as shown here, the actual number of neuropeptide precursors in this transcriptome is considerably larger and analyzing whole genomes reveals additional neuropeptide genes that are not represented in the assembled transcriptomes. While this work was in progress the genome of the Myriapod Strigamia maritima was also published (Chipman et al., 2014). I included this genome in the analysis as the phylogenetic position of the Myriapods falls between insects and Chelicerates (Fig. 1). I felt it would be interesting to have Protostomian outgroups in the phylogenetic analysis of GPCRs, as it was expected that the more recently shared ancestry might lead to better resolved phylogenetic trees. I, therefore, also predicted the neuropeptide GPCRs from the genome of the mollusk Lottia gigantea (Simakov et al., 2013), a species from which a large number of neuropeptide genes has previously been described (Veenstra, 2010, Roch et al., 2011, Mirabeau and Joly, 2013). More recently a large number of GPCRs from the annelid Platynereis dumerilii were published, some of which were deorphanized (Bauknecht and Jékely, 2015). Given the interest of this data set together with the previously published list of putative neuropeptide precursors from this species (Conzelmann et al., 2013) those GPCR sequences were also included in the analysis. Apart from discovering a few novel putative Arthropod neuropeptide genes, the more interesting findings are that many spider and scorpion genes encoding neuropeptides and their receptors have been duplicated, perhaps the result of one or more whole genome duplications.