Dataset Information

Species-specific chemosensory gene expression in the olfactory organs of the malaria vector Anopheles gambiae.

ABSTRACT:

Background

The malaria mosquito Anopheles gambiae has a high preference for human hosts, a characteristic that contributes greatly to its capacity for transmitting human malaria. A sibling species, An. quadriannulatus, has a quite different host preference and feeds mostly on bovids. For this reason it does not contribute to human malaria transmission. Host seeking in mosquitoes is modulated by the olfactory system, which is primarily housed in the antennae and maxillary palps. Therefore, the detection of differing host odors by sibling species may be reflected in the expression level of the olfactory genes involved. Accordingly, we compared the transcriptomes of the antennae and maxillary palps of An. gambiae and An. quadriannulatus.

Results

We identified seven relatively abundant olfactory receptors, nine ionotropic receptors and three odorant binding proteins that are substantially up-regulated in An. gambiae antennae. Interestingly, we find that the maxillary palps of An. gambiae contain a species-specific olfactory receptor, Or52, and five An. gambiae-specific gustatory receptors (AgGr48-52) that are relatively abundant. These five gustatory receptors are also expressed in An. gambiae antennae, although at lower level, indicating a likely role in olfaction, rather than gustation. We also document an approximately three-fold higher overall expression of olfaction genes in the maxillary palps of An. quadriannulatus, indicating an important role of this organ in the olfaction system of this species. Finally, the expression of the CO2 receptor genes is five to six-fold higher in the zoophilic An. quadriannulatus, implying a much higher sensitivity for detecting CO2.

Conclusions

These results identify potential human host preference genes in the malaria vector An. gambiae. Interestingly, species-specific expression of several gustatory receptors in the olfactory organs indicate a role in olfaction rather than gustation. Additionally, a more expansive role for maxillary palps in olfaction is implicated than previously thought, albeit more so in the zoophilic An. quadriannulatus.

SUBMITTER: Hodges TK

PROVIDER: S-EPMC4299676 | biostudies-literature | 2014 Dec

REPOSITORIES: biostudies-literature

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Publications

Species-specific chemosensory gene expression in the olfactory organs of the malaria vector Anopheles gambiae.

Hodges Theresa K TK Cosme Luciano V LV Athrey Giridhar G Pathikonda Sharmila S Takken Willem W Slotman Michel A MA

BMC genomics 20141211

<h4>Background</h4>The malaria mosquito Anopheles gambiae has a high preference for human hosts, a characteristic that contributes greatly to its capacity for transmitting human malaria. A sibling species, An. quadriannulatus, has a quite different host preference and feeds mostly on bovids. For this reason it does not contribute to human malaria transmission. Host seeking in mosquitoes is modulated by the olfactory system, which is primarily housed in the antennae and maxillary palps. Therefore ...[more]

PMID: 25495232

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Project description:Ammonia is one of the principal kairomones originating from human and other animal emanations and in that context, plays an essential role in the host-seeking behaviors of the malaria vector mosquito Anopheles gambiae. Nevertheless, despite its importance in directing host-seeking, the mechanisms underlying ammonia detection in the mosquito olfactory system remains largely unknown. In addition to ongoing efforts to identify and characterize the molecular receptors that underlie ammonia sensitivity, previous studies have revealed a prominent role for ammonium transporters (Amt) in modulating antennal and behavioral responses in Drosophila melanogaster and An. gambiae. In the former, localization of DmAmt in antennal sensilla to auxiliary cells surrounding the ammonia sensory neurons led to the hypothesis that its role was to clear excess ammonium ions in the sensillar lymph. In the latter, RT-PCR and heterologous expression have been used to examine the expression and functional characteristics of the An. gambiae ammonium transporter, AgAmt. We now employ advanced transgenic tools to comprehensively examine AgAmt spatial localization across the peripheral chemosensory appendages in larvae and adult female An. gambiae. In the larval antennae, AgAmt appears localized in both neuronal and auxiliary cells. In contrast to D. melanogaster, in the adult antennae, AgAmt-derived signals are observed in both non-neuronal auxiliary cells and in sensory neurons in ammonia-responsive basiconic and coeloconic sensilla. In the maxillary palps, labella, and tarsi, AgAmt appears restricted to sensory neurons. We have also characterized the responses to ammonia of adult antennal coeloconic sensilla and maxillary palp capitate pegs revealing a correlation between sensillar AgAmt expression and ammonia sensitivity. Taken together, these data suggest that AgAmt may play heterogeneous roles in the adult and larval chemosensory apparatus and potentially broad utility as a supra-receptor target in mosquito control.

Project description:BackgroundAnopheles (An.) coluzzii, one of Africa's primary malaria vectors, is highly anthropophilic. This human host preference contributes greatly to its ability to transmit malaria. In contrast, the closely related An. quadriannulatus prefers to feed on bovids and is not thought to contribute to malaria transmission. The diverged preference for host odor profiles between these sibling species is likely reflected in chemosensory gene expression levels in the olfactory organs. Therefore, we compared the transcriptomes of the antennae and maxillary palps between An. coluzzii and An. quadriannulatus, focusing on the major chemosensory gene families.ResultsWhile chemosensory gene expression is strongly correlated between the two species, various chemosensory genes show significantly enhanced expression in one of the species. In the antennae of An. coluzzii the expression of six olfactory receptors (Ors) and seven ionotropic receptors (Irs) is considerably enhanced, whereas 11 Ors and 3 Irs are upregulated in An. quadriannulatus. In the maxillary palps, leaving aside Irs with very low level of expression, one Ir is strongly enhanced in each species. In addition, we find divergence in odorant binding protein (Obp) gene expression, with several highly expressed Obps being enhanced in the antennae and palps of An. coluzzii. Finally, the expression of several gustatory receptors (Grs) in the palps appears to be species-specific, including a homolog of a sugar-sensing Drosophila Gr.ConclusionsA considerable number of Ors and Irs are differentially expressed between these two closely related species with diverging host preference. These chemosensory genes could play a role in the human host preference of the malaria vector An. coluzzii. Additionally, divergence in Obp expression between the two species suggests a possible role of these odor carrier proteins in determining host preference. Finally, divergence in chemosensory expression in the palps may point towards a possible role for the maxillary palps in host differentiation.

Project description:BACKGROUNDChemosensory signal transduction guides the behavior of many insects, including Anopheles gambiae, the major vector for human malaria in sub-Saharan Africa. To better understand the molecular basis of mosquito chemosensation we have used whole transcriptome RNA sequencing (RNA-seq) to compare transcript expression profiles between the two major chemosensory tissues, the antennae and maxillary palps, of adult female and male An. gambiae.RESULTSWe compared chemosensory tissue transcriptomes to whole body transcriptomes of each sex to identify chemosensory enhanced genes. In the six data sets analyzed, we detected expression of nearly all known chemosensory genes and found them to be highly enriched in both olfactory tissues of males and females. While the maxillary palps of both sexes demonstrated strict chemosensory gene expression overlap, we observed acute differences in sensory specialization between male and female antennae. The relatively high expression levels of chemosensory genes in the female antennae reveal its role as an organ predominately assigned to chemosensation. Remarkably, the expression of these genes was highly conserved in the male antennae, but at much lower relative levels. Alternatively, consistent with a role in mating, the male antennae displayed significant enhancement of genes involved in audition, while the female enhancement of these genes was observed, but to a lesser degree.CONCLUSIONSThese findings suggest that the chemoreceptive spectrum, as defined by gene expression profiles, is largely similar in female and male An. gambiae. However, assuming sensory receptor expression levels are correlated with sensitivity in each case, we posit that male and female antennae are perceptive to the same stimuli, but possess inverse receptive prioritizations and sensitivities. Here we have demonstrated the use of RNA-seq to characterize the sensory specializations of an important disease vector and grounded future studies investigating chemosensory processes.

Dataset Information

Species-specific chemosensory gene expression in the olfactory organs of the malaria vector Anopheles gambiae.

Background

Results

Conclusions

Publications

Species-specific chemosensory gene expression in the olfactory organs of the malaria vector Anopheles gambiae.

Similar Datasets

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