Comparison of transcriptomes from two chemosensory organs in four decapod crustaceans reveals hundreds of candidate chemoreceptor proteins

Abstract

Crustaceans express genes for at least three classes of putative chemosensory proteins. These are: Ionotropic Receptors (IRs), derived from the heterotetrameric ionotropic glutamate receptors (iGluRs); Transient Receptor Potential (TRP) channels, a diverse set of sensor-channels that include several families of chemoreceptor channels; and Gustatory Receptor Like receptors (GRLs), ionotropic receptors that are homologues of Gustatory Receptors (GRs) of insects and are expressed sparingly in most crustaceans so far studied. IRs are typically numerically the most dominant of these receptor proteins in crustaceans and include two classes: co-receptor IRs, which are necessary for making a functional receptor-channel; and tuning IRs, whose specific combination in the IR subunits in the heterotetramer confers chemical specificity. Previous work showed that the transcriptomes from two major chemosensory organs-the lateral flagellum of the antennule (LF) and the tips of the legs (dactyls)-of the Caribbean spiny lobster Panulirus argus express four coreceptor IRs and over 100 tuning IRs. In this paper, we examined and compared the transcriptomes from the LF and dactyls of P. argus and three other decapod crustaceans-the clawed lobster Homarus americanus, red swamp crayfish Procambarus clarkii, and the blue crab Callinectes sapidus. Each species has at least ca. 100 to 250 IRs, 1 to 4 GRLs, and ca. 15 TRP channels including those shown to be involved in chemoreception in other species. The IRs show different degrees of phylogenetic conservation: some are arthropod-conserved, others are pancrustacean-conserved, others appear to be crustacean-conserved, and some appear to be species-specific. Many IRs appear to be more highly expressed in the LF than dactyl. Our results show that decapod crustaceans express an abundance of

A chromosome‐level genome of the mud crab (Scylla paramamosain estampador) provides insights into the evolution of chemical and light perception in this crustacean

“…No ORs are found in the S. paramamosain genome, which is consistent with the hypothesis that ORs emerged at the base of the insect phylogeny (Eyun et al, 2017; Robertson, 2019). Unlike D. pulex (Peñalva‐Arana et al, 2009) and H. azteca (Poynton et al, 2018), all four decapods seem to exhibit much lower GR numbers, and similar results have been found in the transcriptomes of four other decapods (Kozma et al, 2020).…”

“…The expansion of divergent IR genes in the Periplaneta americana genome was assumed to be correlated with its adaptation to urban environments (Li et al, 2018). However, unlike P. americana , most of the expanded IRs in decapods seem to belong to the antennal type in crustaceans or insects, as indicated by phylogenetic analysis; this conclusion is supported by transcriptome analyses in other decapods, in which many IRs are highly expressed in the lateral flagellum of the antennule (Groh et al, 2013; Groh‐Lunow et al, 2014; Kozma et al, 2020), and also supported by qRT‐PCR analysis in this study. Therefore, we hypothesized that S. paramamosain and other decapods, but not nondecapod crustaceans, might mainly use IRs to perceive chemicals.…”

Comparative morphological and transcriptomic analyses reveal chemosensory genes in the poultry red mite, Dermanyssus gallinae

“…A similar finding was observed in the American dog tick Dermacentor variabilis with foreleg-biased expression of GPCRs, suggesting that tick olfaction via the Haller’s organ involves a GPCR-mediated pathway like that of vertebrates and nematodes 29 . In crustaceans, like other non-insect arthropods, GPCRs might be possible candidates for chemoreceptor proteins 39 . We thus suggest that mite olfactory receptors might represent a completely novel type of 7-transmembrane receptor (7TM) family proteins that have yet to be identified.…”

G protein-coupled receptors as candidates for modulation and activation of the chemical senses in decapod crustaceans

“…All analyses were performed on de novo transcriptomes that were previously generated by Kozma et al 2020a [ 40 ]. Full details about animals, organ collection, RNA isolation, and RNA sequencing are described in Kozma et al 2018 and 2020a [ 39 , 40 ]. In brief, three organ-specific cDNA libraries were generated from P .…”

“…Quality assessment on Agilent Bioanalyzer2000 and TapeStation of total RNA extracted, mRNA specific cDNA synthesis, and cDNA paired-end sequencing on the Illumina HiSeq 2500 high-throughput sequencer were performed by Beckman Coulter Genomics (now part of GENEWIZ, South Plainfield, New Jersey) as previously described in Kozma et al 2018 and 2020a [ 39 , 40 ]. For P .…”