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Ignell, R.

Publications and source records attributed to Ignell, R..

7 recordsLinked to original sources

Circadian oscillation of perireceptor events influence olfactory sensitivity in diurnal and nocturnal mosquitoes

Olfaction and circadian rhythm gate different behaviors in mosquitoes that are important for their capacity to transmit disease. However, the mechanisms of odor detection, and the circadian-guided changes in olfactory sensitivity across different mosquito species, remain largely unexplored. To this end, we performed a circadian-dependent RNA-sequencing study of the peripheral olfactory- and brain tissues of female Anopheles culicifacies and Aedes aegypti mosquitoes. Data analysis revealed a significant upregulation of genes encoding: (a) odorant binding proteins (OBPs), required for transportation of odorant molecules towards the olfactory receptors, and (b) xenobiotic-metabolizing enzymes (XMEs) during the day time in Aedes aegypti and during the dusk-transition phase in Anopheles culicifacies. While XMEs primarily function in the elimination of toxic xenobiotics, concurrent elevation of XMEs and OBPs are hypothesized to act cumulatively to regulate perireceptor events and odorant sensitivity. Electroantennographic analysis with both Anopheles gambiae and Aedes aegypti against diverse behaviorally relevant odorants, combined with XMEs inhibitors and RNA interference, establish the proof-of-concept that XMEs function in perireceptor events during odorant detection and influence the odorant sensitivity in mosquitoes. Additionally, the RNA-sequencing and RNAi-mediated knockdown data revealed that daily temporal modulation of neuronal serine proteases may facilitate the consolidation of the brain function, and influence the odor detection process in both diurnal and nocturnal mosquitoes. These findings provide the impetus to further explore the species-specific rhythmic expression pattern of the neuro-olfactory encoded molecular factors, which could pave the way to develop and implement successful mosquito control methods. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=108 SRC="FIGDIR/small/563057v1_ufig1.gif" ALT="Figure 1"> View larger version (49K): org.highwire.dtl.DTLVardef@181b845org.highwire.dtl.DTLVardef@168f22dorg.highwire.dtl.DTLVardef@f3994aorg.highwire.dtl.DTLVardef@d4fc06_HPS_FORMAT_FIGEXP M_FIG C_FIG HighlightsO_LICircadian oscillation of perireceptor proteins possibly influences time-of-day dependent change olfactory sensitivity in diurnal and nocturnal mosquitoes C_LIO_LIDiurnal and nocturnal mosquitoes depict distinct dynamic change in perireceptor proteins C_LIO_LIInhibition of cytochrome P450 gene minimizes antennal response to different odorants C_LIO_LINeuronal serine protease may consolidate brain function and odor detection C_LI

molecular biology↗

The paradox of plant preference: the malaria vectors Anopheles gambiae and Anopheles coluzzii select suboptimal food sources for their survival and reproduction

Anopheles gambiae s.l. mosquitoes, the primary malaria vectors in sub-Saharan Africa, exhibit selectivity among plant species as potential food sources. However, it remains unclear if their preference aligns with optimal nutrient intake and survival. Following an extensive screening of the effects of 31 plant species on An. coluzzii in Burkina Faso, we selected three species for their contrasting effects on mosquito survival, namely Ixora coccinea, Caesalpinia pulcherrima and Combretum indicum. We assessed the sugar content of these plants and their impact on mosquito fructose-positivity, survival, and insemination rate, using Anopheles coluzzii and Anopheles gambiae, and with glucose 5% and water as controls. Plants displayed varying sugar content and differentially affected the survival, sugar intake and insemination rate of mosquitoes. All three plants were more attractive to mosquitoes than controls, with An. gambiae being more responsive than An. coluzzii. Notably, C. indicum was the most attractive but had the lowest sugar content and offered the lowest survival, insemination rate, and fructose positivity. Our findings unveil a performance-preference mismatch in An. coluzzii and An. gambiae regarding plant food sources. Several possible reasons for this negative correlation between performance and preference are discussed.

ecology↗

The evolution of borneol repellency in culicine mosquitoes

The use of essential oils derived from the camphor tree to repel mosquitoes is an ancient practice that originated in Southeast Asia and gradually spread to China and across Europe via the Maritime Silk Road. The olfactory mechanisms by which these oils elicit avoidance behavior are unclear. Here we show that plant bicyclic monoterpenoids and borneol specifically activate a neural pathway that originates in the orphan olfactory receptor neuron of the capitate peg sensillum in the maxillary palp, and projects to the mediodorsal glomerulus 3 in the antennal lobe. This neuron co-locates with two olfactory receptor neurons tuned to carbon dioxide and octenol that mediate human-host detection. We also confirm that borneol elicits repellency against human-seeking female mosquitoes. Understanding the functional role of the mosquito maxillary palp is essential to investigating olfactory signal integration and host-selection behavior.

evolutionary biology↗

De novo transcriptome sequencing of the northern fowl mite, Ornithonyssus sylviarum, shed light into parasitiform poultry mites evolution and its chemoreceptor repertoires

The poultry red mite (PRM), Dermanyssus gallinae (De Geer), and the northern fowl mite (NFM), Ornithonyssus sylviarum (Canestrini and Fanzago), are the most serious pests of poultry, both of which have an expanding global prevalence. Research on NFM has been constrained by a lack of genomic and transcriptomic data. Here, we report and analyze the first transcriptome data for this species. A total of 28,999 unigenes were assembled, of which 19,750 (68.10%) were annotated using seven functional databases. The biological function of these unigenes was predicted using the GO, KOG, and KEGG databases. To gain insight into the chemosensory receptor-based system of parasitiform mites, we furthermore assessed the gene repertoire of gustatory receptors (GRs) and ionotropic receptors (IRs), both of which encode putative ligand-gated ion channel proteins. While these receptors are well characterized in insect model species, our understanding of chemosensory detection in mites and ticks is in its infancy. To address this paucity of data, we identified 9 IR/iGluRs and 2 GRs genes by analyzing transcriptome data in the NFM, while 9 GRs and 41 IR/iGluRs genes were annotated in the PRM genome. Taken together, the transcriptomic and genomic annotation of these two species provide a valuable reference for studies of parasitiform mites, and also helps to understand how chemosensory gene family expansion/contraction events may have been reshaped by an obligate parasitic lifestyle compared with their free-living closest relatives. Future studies should include additional species to validate this observation, and functional characterization of the identified proteins as a step forward in identifying tools for controlling these poultry pests.

molecular biology↗

Comparative dissection of the peripheral olfactory system of the Chagas disease vectors Rhodnius prolixus and Rhodnius brethesi

American trypanosomiasis or Chagas disease is thought to be transmitted by both domestic and sylvatic species of Triatominae. These haematophagous insects use sensory cues to find their vertebrate hosts. Among them, odorants have been shown to play a key role. Previous work revealed morphological differences in the sensory apparatus of sylvatic and domestic species of Triatomines, but to date a functional study of the olfactory system is not available. After examining the antennal sensilla with scanning electronic microscopy (SEM), we compared olfactory responses of the domestic Rhodnius prolixus and the sylvatic Rhodnius brethesi with an electrophysiological approach. In electroantennogram (EAG) recordings, we first show that the antenna of R. prolixus shows high responses to carboxylic acids, compounds found in their habitat and headspace of hosts. We then compared responses from olfactory sensory neurons (OSNs) housed in the grooved peg sensilla of both species as these are tuned to these compounds using single-sensillum recordings (SSR). In R. prolixus, the SSR responses revealed a narrower tuning breath than its sylvatic counterpart, with the latter showing responses to a broader range of chemical classes. Additionally, we observed significant differences between these two species in their response to particular volatiles, such as amyl acetate and butyryl chloride. In summary, the closely related, but ecologically differentiated R. prolixus and R. brethesi display distinct differences in their olfactory functions. Considering the ongoing rapid destruction of the natural habitat of sylvatic species and likely shifts towards environments shaped by humans, we expect that our results will contribute to the design of efficient vector control strategies in the future. Author SummaryAmerican Tripanosomiasis, also known as Chagas disease, is a disease which no one speaks out, although there are up to eight million people infected worldwide. Its causative agent is the protozoan Tripanosoma cruzi which is transmitted by triatomine insects, alias kissing bugs. Several studies have highlighted the importance of olfaction for host-seeking behavior in these insects, which enables them to target their vertebrate hosts, and to get their vital blood meal, while infecting them at the same time. Vector control strategies have been the most efficient policy to combat the spread of Chagas disease by triatomine insects. However, recent changes in the natural habitats of these insects challenge their effectiveness, as species so far thought to be exclusive to sylvatic environments are now frequently found in peridomestic areas. In this context, to understand how sylvatic and domestic kissing bugs detect odors to locate their host and choose their habitats is highly relevant. In this study, we compare the olfactory system of the domestic kissing bug Rhodnius prolixus and its sylvatic counterpart Rhodnius brethesi at a morphological and functional level. We reveal that detection of host and habitat volatiles share many similarities, but also exhibit pronounced differences between both species.

ecology↗

Malaria mosquitoes acquire and allocate cattle urine to enhance life history traits

Nutrient acquisition and allocation integrate foraging and life-history traits in insects. To compensate for the lack of a particular nutrient at different life stages, insects may acquire these through supplementary feeding on e.g., vertebrate secretions, in a process known as puddling. The mosquito Anopheles arabiensis emerges undernourished, and as such, requires nutrients for both metabolism and reproduction. Host-seeking and blood-fed An. arabiensis are attracted to the natural and synthetic odour of cattle urine, which signals a source of nutrients, but not the presence of a host or oviposition site. Females actively imbibe cattle urine, and its main nitrogenous compound, urea, and allocate these resources according to life history trade-offs to flight, survival or reproduction, as a function of physiological state. As a consequence, this behaviour affects vectorial capacity by increasing daily survival and vector density, and thus should be considered in future models. Future vector management strategies are discussed.

ecology↗

Comparative morphological and transcriptomic analyses reveal novel chemosensory genes in the poultry red mite, Dermanyssus gallinae and knockdown by RNA interference

Detection of chemical cues via chemosensory receptor proteins are essential for most animals, and underlies critical behaviors, including location and discrimination of food resources, identification of sexual partners and avoidance of predators. The current knowledge of how chemical cues are detected is based primarily on data acquired from studies on insects, while our understanding of the molecular basis for chemoreception in acari, mites in particular, remains limited. The poultry red mite (PRM), Dermanyssus gallinae, is one of the most important blood-feeding ectoparasites of poultry. Unlike other ectoparasites on animals, PRM feeds mainly at night. During daytime, these animals hide themselves in crevices around the poultry house. The diversity in habitat usage, as well as the demonstrated host finding and avoidance behaviors suggest that PRM relies on their sense of smell to orchestrate complex behavioral decisions. Comparative transcriptome analyses revealed the presence of candidate variant ionotropic receptors (IRs), odorant binding proteins (OBPs), niemann-pick proteins type C2 (NPC2) and sensory neuron membrane proteins (SNMPs). Some of these proteins were highly and differentially expressed in the forelegs of PRM. Rhodopsin-like G protein-coupled receptors (GPCRs) were also identified, while insect-specific odorant receptors (ORs) and odorant co-receptors (ORcos) were not detected. Furthermore, using scanning electron microscopy (SEM), the tarsomeres of all legs pairs were shown to be equipped with sensilla chaetica with or without tip pores, while wall-pored olfactory sensilla chaetica were restricted to the distal-most tarsomeres of the forelegs. Further, using the conserved odorant binding protein (OBP) as a test case, the results showed that RNA interference (RNAi) can be induced in D. gallinae chemosensory tissues. This study is the first to describe the presence of chemosensory genes in any Dermanyssidae family. It is also the first report of chemosensory gene knockdown by RNAi in any mite species and demonstrate that their diminutive size, less than 1 mm, is not a major impediment when applying gene knockdown approaches. Our findings make a significant step forward in understanding the chemosensory abilities of D. gallinae.

molecular biology↗