Deciphering the olfactory repertoire of the tiger mosquito  Aedes albopictus

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Abstract

Background

The Asian tiger mosquito Aedes albopictus is a highly invasive species and competent vector of several arboviruses (e.g. dengue, chikungunya, Zika) and parasites (e.g. dirofilaria) of public health importance. Compared to other mosquito species, Ae. albopictus females exhibit a generalist host seeking as well as a very aggressive biting behaviour that are responsible for its high degree of nuisance. Several complex mosquito behaviours such as host seeking, feeding, mating or oviposition rely on olfactory stimuli that target a range of sensory neurons localized mainly on specialized head appendages such as antennae, maxillary palps and the mouthparts.

Results

With the aim to describe the Ae. albopictus olfactory repertoire we have used RNA-seq to reveal the transcriptome profiles of female antennae and maxillary palps. Male heads and whole female bodies were employed as reference for differential expression analysis. The relative transcript abundance within each tissue (TPM, transcripts per kilobase per million) and the pairwise differential abundance in the different tissues (fold change values and false discovery rates) were evaluated. Contigs upregulated in the antennae (620) and maxillary palps (268) were identified and relative GO and PFAM enrichment profiles analysed. Chemosensory genes were described: overall, 77 odorant binding proteins (OBP), 82 odorant receptors (OR), 60 ionotropic receptors (IR) and 30 gustatory receptors (GR) were identified by comparative genomics and transcriptomics. In addition, orthologs of genes expressed in the female/male maxillary palps and/or antennae and involved in thermosensation (e.g. pyrexia and arrestin1), mechanosensation (e.g. piezo and painless) and neuromodulation were classified.

Conclusions

We provide here the first detailed transcriptome of the main Ae. albopictus sensory appendages, i.e. antennae and maxillary palps. A deeper knowledge of the olfactory repertoire of the tiger mosquito will help to better understand its biology and may pave the way to design new attractants/repellents.

Electronic supplementary material

The online version of this article (10.1186/s12864-017-4144-1) contains supplementary material, which is available to authorized users.

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Most cited references 80

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Insect olfactory receptors are heteromeric ligand-gated ion channels.

Koji Sato, Maurizio Pellegrino, Takao Nakagawa … (2008)

In insects, each olfactory sensory neuron expresses between one and three ligand-binding members of the olfactory receptor (OR) gene family, along with the highly conserved and broadly expressed Or83b co-receptor. The functional insect OR consists of a heteromeric complex of unknown stoichiometry but comprising at least one variable odorant-binding subunit and one constant Or83b family subunit. Insect ORs lack homology to G-protein-coupled chemosensory receptors in vertebrates and possess a distinct seven-transmembrane topology with the amino terminus located intracellularly. Here we provide evidence that heteromeric insect ORs comprise a new class of ligand-activated non-selective cation channels. Heterologous cells expressing silkmoth, fruitfly or mosquito heteromeric OR complexes showed extracellular Ca2+ influx and cation-non-selective ion conductance on stimulation with odorant. Odour-evoked OR currents are independent of known G-protein-coupled second messenger pathways. The fast response kinetics and OR-subunit-dependent K+ ion selectivity of the insect OR complex support the hypothesis that the complex between OR and Or83b itself confers channel activity. Direct evidence for odorant-gated channels was obtained by outside-out patch-clamp recording of Xenopus oocyte and HEK293T cell membranes expressing insect OR complexes. The ligand-gated ion channel formed by an insect OR complex seems to be the basis for a unique strategy that insects have acquired to respond to the olfactory environment.

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Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels.

Dieter Wicher, Ronny Schäfer, René Bauernfeind … (2008)

From worm to man, many odorant signals are perceived by the binding of volatile ligands to odorant receptors that belong to the G-protein-coupled receptor (GPCR) family. They couple to heterotrimeric G-proteins, most of which induce cAMP production. This second messenger then activates cyclic-nucleotide-gated ion channels to depolarize the olfactory receptor neuron, thus providing a signal for further neuronal processing. Recent findings, however, have challenged this concept of odorant signal transduction in insects, because their odorant receptors, which lack any sequence similarity to other GPCRs, are composed of conventional odorant receptors (for example, Or22a), dimerized with a ubiquitously expressed chaperone protein, such as Or83b in Drosophila. Or83b has a structure akin to GPCRs, but has an inverted orientation in the plasma membrane. However, G proteins are expressed in insect olfactory receptor neurons, and olfactory perception is modified by mutations affecting the cAMP transduction pathway. Here we show that application of odorants to mammalian cells co-expressing Or22a and Or83b results in non-selective cation currents activated by means of an ionotropic and a metabotropic pathway, and a subsequent increase in the intracellular Ca(2+) concentration. Expression of Or83b alone leads to functional ion channels not directly responding to odorants, but being directly activated by intracellular cAMP or cGMP. Insect odorant receptors thus form ligand-gated channels as well as complexes of odorant-sensing units and cyclic-nucleotide-activated non-selective cation channels. Thereby, they provide rapid and transient as well as sensitive and prolonged odorant signalling.

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Insect glutathione transferases and insecticide resistance.

A A Enayati, H Ranson, J Hemingway (2005)

Glutathione transferases (GSTs) are a diverse family of enzymes found ubiquitously in aerobic organisms. They play a central role in the detoxification of both endogenous and xenobiotic compounds and are also involved in intracellular transport, biosynthesis of hormones and protection against oxidative stress. Interest in insect GSTs has primarily focused on their role in insecticide resistance. GSTs can metabolize insecticides by facilitating their reductive dehydrochlorination or by conjugation reactions with reduced glutathione, to produce water-soluble metabolites that are more readily excreted. In addition, they contribute to the removal of toxic oxygen free radical species produced through the action of pesticides. Annotation of the Anopheles gambiae and Drosophila melanogaster genomes has revealed the full extent of this enzyme family in insects. This mini review describes the insect GST enzyme family, focusing specifically on their role in conferring insecticide resistance.

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Author and article information

Contributors

Fabrizio Lombardo:

ORCID: http://orcid.org/0000-0002-8563-0612

fabrizio.lombardo@uniroma1.it

Marco Salvemini: marco.salvemini@unina.it

Carmine Fiorillo: carmine_fiorillo@hotmail.it

Tony Nolan: t.nolan@imperial.ac.uk

Laurence J. Zwiebel: l.zwiebel@vanderbilt.edu

José M. Ribeiro: jribeiro@niaid.nih.gov

Bruno Arcà: bruno.arca@uniroma1.it

Journal

Journal ID (nlm-ta): BMC Genomics

Journal ID (iso-abbrev): BMC Genomics

Title: BMC Genomics

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2164

Publication date (Electronic): 11 October 2017

Publication date PMC-release: 11 October 2017

Publication date Collection: 2017

Volume: 18

Electronic Location Identifier: 770

Affiliations

[1 ]GRID grid.7841.a, Department of Public Health and Infectious Diseases, Division of Parasitology, , Sapienza University of Rome, ; Rome, Italy

[2 ]ISNI 0000 0001 0790 385X, GRID grid.4691.a, Department of Biology, , University of Naples Federico II, ; Naples, Italy

[3 ]ISNI 0000 0001 2113 8111, GRID grid.7445.2, Department of Life Sciences, , Imperial College London, ; London, UK

[4 ]ISNI 0000 0001 2264 7217, GRID grid.152326.1, Department of Biological Sciences, , Vanderbilt University, ; Nashville, TN USA

[5 ]ISNI 0000 0001 2164 9667, GRID grid.419681.3, NIAID, Laboratory of Malaria and Vector Research, NIH, ; Rockville, 20852 MD USA

Author information

Fabrizio Lombardo http://orcid.org/0000-0002-8563-0612

Article

Publisher ID: 4144

DOI: 10.1186/s12864-017-4144-1

PMC ID: 5637092

PubMed ID: 29020917

SO-VID: 0a30bf76-83a4-4ba0-a73f-3d82efde69c9

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 3 July 2017

Date accepted : 2 October 2017

Funding

Funded by: Sapienza Università di Roma (IT)

Award ID: C26A14AKKH

Award Recipient : Bruno Arcà

Funded by: European Union INFRAVEC

Award ID: 228421

Award Recipient : Fabrizio Lombardo Bruno Arcà

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: mosquito,aedes albopictus,olfaction,antennae,maxillary palps,mrna-sequencing,chemosensory genes

Data availability:

ScienceOpen disciplines: Genetics

Keywords: mosquito, aedes albopictus, olfaction, antennae, maxillary palps, mrna-sequencing, chemosensory genes

Deciphering the olfactory repertoire of the tiger mosquito Aedes albopictus

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Genomic Prediction

Most cited references 80

Insect olfactory receptors are heteromeric ligand-gated ion channels.

Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels.

Insect glutathione transferases and insecticide resistance.

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