The Chemosensory Transcriptome of a Diving Beetle

Insects astoundingly dominate Earth’s land ecosystems and have a huge impact on human life. Almost every aspect of their life relies upon their highly efficient and adaptable chemosensory system. In the air, most chemical signals that are detected at long range are hydrophobic molecules, which insec...

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Autores principales:	Nicolas Montagné, Muriel Jager, Thomas Chertemps, Emma Persyn, Yan Jaszczyszyn, Camille Meslin, Emmanuelle Jacquin-Joly, Michaël Manuel
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	ecological transitions freshwater insects Dytiscidae chemical ecology chemosensory receptors odorant-binding proteins Evolution QH359-425 Ecology QH540-549.5
Acceso en línea:	https://doaj.org/article/2bbe1ff29a98461ea3dab487a0976698
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spelling	oai:doaj.org-article:2bbe1ff29a98461ea3dab487a09766982021-12-03T16:21:51ZThe Chemosensory Transcriptome of a Diving Beetle2296-701X10.3389/fevo.2021.773915https://doaj.org/article/2bbe1ff29a98461ea3dab487a09766982021-12-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fevo.2021.773915/fullhttps://doaj.org/toc/2296-701XInsects astoundingly dominate Earth’s land ecosystems and have a huge impact on human life. Almost every aspect of their life relies upon their highly efficient and adaptable chemosensory system. In the air, most chemical signals that are detected at long range are hydrophobic molecules, which insects detect using proteins encoded by multigenic families that emerged following land colonization by insect ancestors, namely the odorant-binding proteins (OBPs) and the odorant receptors (ORs). However, land-to-freshwater transitions occurred in many lineages within the insect tree of life. Whether chemosensory gene repertoires of aquatic insects remained essentially unchanged or underwent more or less drastic modifications to cope with physico-chemical constraints associated with life underwater remains virtually unknown. To address this issue, we sequenced and analyzed the transcriptome of chemosensory organs of the diving beetle Rhantus suturalis (Coleoptera, Dytiscidae). A reference transcriptome was assembled de novo using reads from five RNA-seq libraries (male and female antennae, male and female palps, and wing muscle). It contained 47,570 non-redundant unigenes encoding proteins of more than 50 amino acids. Within this reference transcriptome, we annotated sequences coding 53 OBPs, 48 ORs, 73 gustatory receptors (GRs), and 53 ionotropic receptors (IRs). Phylogenetic analyses notably revealed a large OBP gene expansion (35 paralogs in R. suturalis) as well as a more modest OR gene expansion (9 paralogs in R. suturalis) that may be specific to diving beetles. Interestingly, these duplicated genes tend to be expressed in palps rather than in antennae, suggesting a possible adaptation with respect to the land-to-water transition. This work provides a strong basis for further evolutionary and functional studies that will elucidate how insect chemosensory systems adapted to life underwater.Nicolas MontagnéMuriel JagerThomas ChertempsEmma PersynYan JaszczyszynCamille MeslinEmmanuelle Jacquin-JolyMichaël ManuelFrontiers Media S.A.articleecological transitionsfreshwater insectsDytiscidaechemical ecologychemosensory receptorsodorant-binding proteinsEvolutionQH359-425EcologyQH540-549.5ENFrontiers in Ecology and Evolution, Vol 9 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	ecological transitions freshwater insects Dytiscidae chemical ecology chemosensory receptors odorant-binding proteins Evolution QH359-425 Ecology QH540-549.5
spellingShingle	ecological transitions freshwater insects Dytiscidae chemical ecology chemosensory receptors odorant-binding proteins Evolution QH359-425 Ecology QH540-549.5 Nicolas Montagné Muriel Jager Thomas Chertemps Emma Persyn Yan Jaszczyszyn Camille Meslin Emmanuelle Jacquin-Joly Michaël Manuel The Chemosensory Transcriptome of a Diving Beetle
description	Insects astoundingly dominate Earth’s land ecosystems and have a huge impact on human life. Almost every aspect of their life relies upon their highly efficient and adaptable chemosensory system. In the air, most chemical signals that are detected at long range are hydrophobic molecules, which insects detect using proteins encoded by multigenic families that emerged following land colonization by insect ancestors, namely the odorant-binding proteins (OBPs) and the odorant receptors (ORs). However, land-to-freshwater transitions occurred in many lineages within the insect tree of life. Whether chemosensory gene repertoires of aquatic insects remained essentially unchanged or underwent more or less drastic modifications to cope with physico-chemical constraints associated with life underwater remains virtually unknown. To address this issue, we sequenced and analyzed the transcriptome of chemosensory organs of the diving beetle Rhantus suturalis (Coleoptera, Dytiscidae). A reference transcriptome was assembled de novo using reads from five RNA-seq libraries (male and female antennae, male and female palps, and wing muscle). It contained 47,570 non-redundant unigenes encoding proteins of more than 50 amino acids. Within this reference transcriptome, we annotated sequences coding 53 OBPs, 48 ORs, 73 gustatory receptors (GRs), and 53 ionotropic receptors (IRs). Phylogenetic analyses notably revealed a large OBP gene expansion (35 paralogs in R. suturalis) as well as a more modest OR gene expansion (9 paralogs in R. suturalis) that may be specific to diving beetles. Interestingly, these duplicated genes tend to be expressed in palps rather than in antennae, suggesting a possible adaptation with respect to the land-to-water transition. This work provides a strong basis for further evolutionary and functional studies that will elucidate how insect chemosensory systems adapted to life underwater.
format	article
author	Nicolas Montagné Muriel Jager Thomas Chertemps Emma Persyn Yan Jaszczyszyn Camille Meslin Emmanuelle Jacquin-Joly Michaël Manuel
author_facet	Nicolas Montagné Muriel Jager Thomas Chertemps Emma Persyn Yan Jaszczyszyn Camille Meslin Emmanuelle Jacquin-Joly Michaël Manuel
author_sort	Nicolas Montagné
title	The Chemosensory Transcriptome of a Diving Beetle
title_short	The Chemosensory Transcriptome of a Diving Beetle
title_full	The Chemosensory Transcriptome of a Diving Beetle
title_fullStr	The Chemosensory Transcriptome of a Diving Beetle
title_full_unstemmed	The Chemosensory Transcriptome of a Diving Beetle
title_sort	chemosensory transcriptome of a diving beetle
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/2bbe1ff29a98461ea3dab487a0976698
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The Chemosensory Transcriptome of a Diving Beetle

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