Comparative Genomics Reveals Thousands of Novel Chemosensory Genes and Massive Changes in Chemoreceptor Repertories across Chelicerates

Genome Biology and Evolution, May 2018

Chemoreception is a widespread biological function that is essential for the survival, reproduction, and social communication of animals. Though the molecular mechanisms underlying chemoreception are relatively well known in insects, they are poorly studied in the other major arthropod lineages. Current availability of a number of chelicerate genomes constitutes a great opportunity to better characterize gene families involved in this important function in a lineage that emerged and colonized land independently of insects. At the same time, that offers new opportunities and challenges for the study of this interesting animal branch in many translational research areas. Here, we have performed a comprehensive comparative genomics study that explicitly considers the high fragmentation of available draft genomes and that for the first time included complete genome data that cover most of the chelicerate diversity. Our exhaustive searches exposed thousands of previously uncharacterized chemosensory sequences, most of them encoding members of the gustatory and ionotropic receptor families. The phylogenetic and gene turnover analyses of these sequences indicated that the whole-genome duplication events proposed for this subphylum would not explain the differences in the number of chemoreceptors observed across species. A constant and prolonged gene birth and death process, altered by episodic bursts of gene duplication yielding lineage-specific expansions, has contributed significantly to the extant chemosensory diversity in this group of animals. This study also provides valuable insights into the origin and functional diversification of other relevant chemosensory gene families different from receptors, such as odorant-binding proteins and other related molecules.

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Comparative Genomics Reveals Thousands of Novel Chemosensory Genes and Massive Changes in Chemoreceptor Repertories across Chelicerates

Advance Access publication April Comparative Genomics Reveals Thousands of Novel Chemosensory Genes and Massive Changes in Chemoreceptor Repertories across Chelicerates Joel Vizueta 0 Julio Rozas ; 0 Alejandro Sanchez-Gracia 0 0 Departament de Gene` tica, Microbiologia i Estadıstica and Institut de Recerca de la Biodiversitat (IRBio), Facultat de Biologia, Universitat de Barcelona , Barcelona , Spain Chemoreception is a widespread biological function that is essential for the survival, reproduction, and social communication of animals. Though the molecular mechanisms underlying chemoreception are relatively well known in insects, they are poorly studied in the other major arthropod lineages. Current availability of a number of chelicerate genomes constitutes a great opportunity to better characterize gene families involved in this important function in a lineage that emerged and colonized land independently of insects. At the same time, that offers new opportunities and challenges for the study of this interesting animal branch in many translational research areas. Here, we have performed a comprehensive comparative genomics study that explicitly considers the high fragmentation of available draft genomes and that for the first time included complete genome data that cover most of the chelicerate diversity. Our exhaustive searches exposed thousands of previously uncharacterized chemosensory sequences, most of them encoding members of the gustatory and ionotropic receptor families. The phylogenetic and gene turnover analyses of these sequences indicated that the whole-genome duplication events proposed for this subphylum would not explain the differences in the number of chemoreceptors observed across species. A constant and prolonged gene birth and death process, altered by episodic bursts of gene duplication yielding lineage-specific expansions, has contributed significantly to the extant chemosensory diversity in this group of animals. This study also provides valuable insights into the origin and functional diversification of other relevant chemosensory gene families different from receptors, such as odorant-binding proteins and other related molecules. chemosensory gene family; gustatory receptors; ionotropic receptors; acari; spiders; scorpions Introduction The i5k initiative (Robinson et al. 2011) has greatly boosted the complete genome sequencing and functional annotation of a number of arthropod species. The currently available genome data were obtained from species chosen for their significance as model organisms in diverse areas, such as agriculture, medicine, food safety or biodiversity, or for their strategic phylogenetic position in evolutionary studies on the diversification of the major arthropod lineages (Adams et al. 2000; Colbourne et al. 2011; Cao et al. 2013; Chipman et al. 2014; Sanggaard et al. 2014; Gulia-Nuss et al. 2016) . As expected, the first sequencing initiatives focused on insects, although the number of sequenced noninsect genomes has increased considerably over time, especially in chelicerates. The recent genome sequence data from chelicerate species (Cao et al. 2013; Sanggaard et al. 2014; Gulia-Nuss et al. 2016) are disrupting the strongly biased taxonomic distribution of arthropod genomes hitherto available. More importantly, these new data have greatly facilitated studies on the origin and evolutionary divergence of this highly diverse animal subphylum (Kenny et al. 2016; Schwager et al. 2017) , which has important impacts on translational research such as silk production in spiders, biomedical applications of spider and scorpion venom toxins, or plague control in acari (Mille et al. 2015; Hoy et al. 2016; Babb et al. 2017; Gendreau et al. 2017; Pennisi 2017) . Chemoreception is a paradigmatic example of a relatively well-known biological system in insects, but it is not as well characterized in other arthropods despite numerous practical applications as pest control strategies, biosensors or electronic nose sensors (Berna et al. 2009; Wei et al. 2017) . In chelicerates, as in other animals, the chemosensory system (CS) is critical for the survival, reproduction, and social communication of individuals. The detection and integration of environmental chemical signals, including smell and taste, allow organisms to detect food, hosts, and predators and frequently play a crucial role in social communication (Joseph and Carlson 2015). In Drosophila, peripheral events occur in specialized hair-like cuticular structures (sesilla) that are distributed throughout the body surface, with a prominent concentration in antennae and maxillary palps (olfactory sensilla) or on the distal tarsal segments of the legs (gustatory sensilla) (Pelosi 1996; Shanbhag et al. 2001) . In this species, chemoreceptor proteins, which are located in the membranes of sensory neurons innervating the sensillum lymph, convert the external chemical signal into an electrical one, which is, (...truncated)


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Vizueta, Joel, Rozas, Julio, Sánchez-Gracia, Alejandro, Alba, Mar. Comparative Genomics Reveals Thousands of Novel Chemosensory Genes and Massive Changes in Chemoreceptor Repertories across Chelicerates, Genome Biology and Evolution, 2018, pp. 1221-1236, Volume 10, Issue 5, DOI: 10.1093/gbe/evy081