Evolution of Chemosensory Gene Families in Arthropods: Insight from the First Inclusive Comparative Transcriptome Analysis Across Spider Appendages
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GBE Evolution of Chemosensory Gene Families in Arthropods: Insight from the First Inclusive Comparative Transcriptome Analysis across Spider Appendages Joel Vizueta1, Cristina Frı´as-Lo´ pez1,NuriaMacı´as-Herna´ndez2,MiquelA.Arnedo2, Alejandro Sa´nchez- Gracia1,*, and Julio Rozas1,* 1Departament de Gene`tica, Microbiologia i Estadı´stica and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Spain 2Departament de Biologia Evolutiva, Ecologia i Cie`ncies Ambientals and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Spain *Corresponding authors: E-mails: [email protected]; [email protected]. Accepted: December 16, 2016 Data deposition: This project has been deposited at the Sequence Read Archive (SRA) database under accession numbers SRX1612801, SRX1612802, SRX1612803 and SRX1612804 (Bioproject number: PRJNA313901). Abstract Unlike hexapods and vertebrates, in chelicerates, knowledge of the specific molecules involved in chemoreception comes exclusively from the comparative analysis of genome sequences. Indeed, the genomes of mites, ticks and spiders contain several genes encoding homologs of some insect membrane receptors and small soluble chemosensory proteins. Here, we conducted for the first time a comprehensive comparative RNA-Seq analysis across different body structures of a chelicerate: the nocturnal wandering hunter spider Dysdera silvatica Schmidt 1981. Specifically, we obtained the complete transcriptome of this species as well as the specific expression profile in the first pair of legs and the palps, which are thought to be the specific olfactory appendages in spiders, and in the remaining legs, which also have hairs that have been morphologically identified as chemosensory. We identified several ionotropic (Ir) and gustatory (Gr) receptor family members exclusively or differentially expressed across transcriptomes, some exhibiting a distinctive pattern in the putative olfactory appendages. Furthermore, these IRs were the only known olfactory receptors identified in such structures. These results, integrated with an extensive phylogenetic analysis across arthropods, uncover a specialization of the chemosensory gene repertoire across the body of D. silvatica and suggest that some IRs likely mediate olfactory signaling in chelicerates. Noticeably, we detected the expression of a gene family distantly related to insect odorant-binding proteins (OBPs), suggesting that this gene family is more ancient than previously believed, as well as the expression of an uncharacterized gene family encoding small globular secreted proteins, which appears to be a good chemosensory gene family candidate. Key words: chemosensory gene families, specific RNA-Seq, de novo transcriptome assembly, functional annotation, chelicerates, arthropods. Introduction sensilla, which can be found almost anywhere in the body Chemoreception, the detection and processing of chemical (Joseph and Carlson 2015). In Drosophila, olfactory sensilla signals in the environment, is a biological process that is critical are concentrated on the antenna and the maxillary palps, for animal survival and reproduction. The essential role of while gustatory sensilla are spread across various body loca- smell and taste in the detection of food, hosts and predators tions, such as the proboscis, the legs and the anterior margins and their participation in social communication make the mo- of wings (Pelosi 1996; Shanbhag et al. 2001). The chemore- lecular components of this system solid candidates for impor- ceptor proteins embedded within the membrane of sensory tant adaptive changes associated with animal terrestrialization neurons (SN) innervating these sensilla are responsible for (Whiteman and Pierce 2008). In insects, chemical recognition transducing the external chemical signal into an action poten- occurs in specialized hair-like cuticular structures called tial. In the case of smell, olfactory SNs project the axons to ß The Author(s) 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] 178 Genome Biol. Evol. 9(1):178–196. doi:10.1093/gbe/evw296 Advance Access publication December 24, 2016 Downloaded from https://academic.oup.com/gbe/article-abstract/9/1/178/2732147 by University of Helsinki, Viikki Science Library user on 12 January 2018 Evolution of Chemosensory Gene Families in Arthropods GBE specific centers of the brain, where the signals are processed been detected to date (Vieira and Rozas 2011; Chipman et al. and engender a behavioral response to the specific external 2014). Overall, available genomic studies suggest that the Ir stimuli. The process can be facilitated by small soluble chemo- gene family is responsible for smell not only in chelicerates but sensory proteins that are secreted in the lymph that bathes the also in all nonneopteran arthropods (Croset et al. 2010; dendrites of the SNs and are believed to solubilize and either Colbourne et al. 2011; Chipman et al. 2014; Gulia-Nuss transport the signaling molecules to membrane receptors or et al. 2016). Regarding taste, the presence of numerous protect them from premature degradation (Vogt and copies of Gr and nonconserved Ir (a group of divergent IR Riddiford 1981; Pelosi et al. 2006). Although insect chemore- proteins associated with gustatory function in insects, Croset ceptors and soluble chemosensory proteins are encoded by et al. 2010) genes in chelicerate genomes clearly suggests that gene families exhibiting high gene turnover rates (see these families are responsible for contact chemoreception in Sa´nchez-Gracia et al. 2011 for a comprehensive review), dis- this species. tant homologues of the members of these families have been Nevertheless, the simple comparative analysis of genomic identified in other arthropod lineages (Colbourne et al. 2011; sequences does not allow inferring which specific members of Vieira and Rozas 2011; Chipman et al. 2014; Frı´as-Lo´ pez et al. already known chemosensory families are involved in the dif- 2015; Gulia-Nuss et al. 2016). Vertebrate functional counter- ferent sensory modalities. Additionally, chelicerates could also parts of these gene families, however, are not evolutionarily use molecules completely different from those already known related; indeed, the members of this subphylum use different in insects during the water-to-land transition, which should molecules to perform the same general physiological function also be different from those used by vertebrates (these mole- (Kaupp 2010). cules have also not been found in the available genome se- Spiders comprise a highly diverse group of arthropods, in- quences); these uncharacterized genes (or annotated with cluding >45,000 described species (World Spider Catalog incomplete gene models) would be not directly detectable 2016), and are dominant predators in most terrestrial ecosys- only by comparative genomics. Instead, specific transcriptomic tems. Given their potential as biological control agents as well analyses of chemosensory tissues can provide useful insight as the engineering properties of silk and venom, these organ- into all these issues. Antennae-specific gene expression studies isms are of great economic and medical relevance (Clarke in lobsters and hermit crabs (Corey et al. 2013; Groh-Lunow et al. 2014). Because the Arachnida ancestors of these cheli- et al. 2014), for example, have revealed the presence of sev- cerates colonized the land ~475 Ma, long after the split of the eral transcripts encoding IRs, supporting the active role in ol- four major extant arthropod lineages (Rota-Stabelli et al. faction of this gene family in crustaceans. To gain insight into 2013), spiders are good models for comparative studies on the specific proteins involved in chelicerate chemoreception, the diverse strategies adopted by arthropod lineages during we recently performed a tissue-specific comparative transcrip- their independent adaptation to terrestrial environments. tomics study in the funnel-web spider Macrothele calpeiana However, despite their biological and translational implica- (Frı´as-Lo´ pez et al. 2015). Unfortunately, we failed to detect tions, there are relatively few genomic and transcriptomic the specific expression of Ir or Gr genes in the first pair of legs studies conducted on these organisms compared with those and in palps, the best candidate structures to hold olfactory conducted on insects, and studies on spiders almost exclu- hairs in chelicerates. This result might be caused by either the sively focus on silk and venom research (Grbic´ et al. 2011; sedentary lifestyle of this mygalomorph spider, which may Clarke et al. 2014; Posnien et al. 2014; Sanggaard et al. 2014). lead to a marginal role of chemical communication in this Spiders can detect volatile and nonvolatile compounds species, or the low sequencing coverage of this RNA-Seq through specialized chemosensitive hairs distributed at the study. tips of various extremities and appendages, including legs Here, in order to better characterize the chemosensory rep- and palps (Foelix 1970; Foelix and Chu-Wang 1973; ertoire of a spider, we report a more comprehensive compar- Kronestedt