Abstract
Decoding the molecular basis of host seeking and blood feeding behavioral evolution/adaptation in the adult female mosquitoes may provide an opportunity to design new molecular strategy to disrupt human-mosquito interactions. Although there is a great progress in the field of mosquito olfaction and chemo-detection, little is known about the sex-specific evolution of the specialized olfactory system of adult female mosquitoes that enables them to drive and manage the complex blood-feeding associated behavioral responses. A comprehensive RNA-Seq analysis of prior and post blood meal olfactory system of An. culicifacies mosquito revealed a minor but unique change in the nature and regulation of key olfactory genes that may play a pivotal role in managing diverse behavioral responses. Based on age-dependent transcriptional profiling, we further demonstrated that adult female mosquito's chemosensory system gradually learned and matured to drive the host-seeking and blood feeding behavior at the age of 5–6 days. A time scale expression analysis of Odorant Binding Proteins (OBPs) unravels unique association with a late evening to midnight peak biting time. Blood meal-induced switching of unique sets of OBP genes and Odorant Receptors (Ors) expression coincides with the change in the innate physiological status of the mosquitoes. Blood meal follows up experiments further provide enough evidence that how a synergistic and concurrent action of OBPs-Ors may drive “prior and post blood meal” associated complex behavioral events. A dominant expression of two sensory appendages proteins (SAP-1 & SAP2) in the legs of An. culicifacies suggests that this mosquito species may draw an extra advantage of having more sensitive appendages than An. stephensi, an urban malarial vector in the Indian subcontinents. Finally, our molecular modeling analysis predicts crucial amino acid residues for future functional characterization of the sensory appendages proteins which may play a central role in regulating multiple behaviors of An. culicifacies mosquito.SIGNIFICANCE Evolution and adaptation of blood feeding behavior not only favored the reproductive success of adult female mosquitoes but also make them important disease-transmitting vectors. An environmental exposure after emergence may favor the broadly tuned olfactory system of mosquitoes to drive complex behavioral responses. But, how these olfactory derived genetic factors manage female specific “pre and post” blood meal associated complex behavioral responses are not well known. Our findings suggest that a synergistic action of olfactory factors may govern an innate to prime learning strategy to facilitate rapid blood meal acquisition and downstream behavioral activities. A species-specific transcriptional profiling and an in-silico analysis predict that “sensory appendages protein” may be a unique target to design disorientation strategy against the mosquito Anopheles culicifacies.
Highlights
Mosquitoes are one of the deadliest living animals, transmitting a variety of infectious diseases such as malaria, dengue fever, chikungunya and zika fever worldwide
To decode and establish the possible molecular relationship managing “prior and post” blood meal behavioral events we developed a working hypothesis (Figure 2), a plausible mechanism which may have a significant influence on mosquito feeding and survival in diverse ecologies
We chose 30 h PBM as a critical time when completion of blood meal digestion occurs in the midgut, which may have a direct influence on the reactivation of the olfactory system (Figure S2) (Gonalves et al, 2009; Rinker et al, 2013; Taparia et al, 2017)
Summary
Mosquitoes are one of the deadliest living animals, transmitting a variety of infectious diseases such as malaria, dengue fever, chikungunya and zika fever worldwide. The well-developed nasal system of mosquitoes is able to detect and discriminate thousands of different odor molecules and play an essential role in the facilitation of olfactory guided behavior These complex behavioral events are largely mediated by the diverse chemosensory genes encoding odorant binding proteins (OBPs), odorant degrading enzymes (ODEs), odorant receptors (Ors) and other accessory proteins including sensory neuron membrane protein (SNMP) (Takken and Knols, 2010). Odorant binding proteins (OBPs), which are bathed within the sensillum lymph, are low molecular weight soluble proteins that mediate the first interaction of the olfactory system with the external world (Takken and Knols, 2010; Carey and Carlson, 2011; Brito et al, 2016). Orco is essential for dendritic trafficking and presentation of the OrX in the membrane and facilitate the formation of odorant gated ion channels by structural alteration that is opened upon odorant binding (Zwiebel and Takken, 2004; Takken and Knols, 2010)
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
