Sex specific molecular responses of quick-to-court protein in Indian malarial vector Anopheles culicifacies : conflict of mating versus blood feeding behaviour

De, Tanwee Das; Sharma, Punita; Rawal, Charu; Kumari, Seena; Tavetiya, Sanjay; Yadav, Jyoti; Hasija, Yasha; Dixit, Rajnikant

doi:10.1016/j.heliyon.2017.e00361

Cited by 9 publications

(5 citation statements)

References 35 publications

(41 reference statements)

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“…Our recent finding suggested that quick-to-court protein may have a crucial role to meet the conflicting demand of sexual mate partner finding and/or a suitable vertebrate host finding by regulating the expression of unknown olfactory genes in adult An. culicifacies mosquito (De et al, 2017 ). In fact, the organization of the olfactory components is morphologically similar in both the sexes but carries unique structural differences which are responsible for discrete temporal peaks of activities to sense swarm and identify sex partner for a successful mating event (Pitts et al, 2011 ).…”

Section: Introductionmentioning

confidence: 99%

A Synergistic Transcriptional Regulation of Olfactory Genes Drives Blood-Feeding Associated Complex Behavioral Responses in the Mosquito Anopheles culicifacies

Thomas

Verma

et al. 2018

Front. Physiol.

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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.

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Section: Introductionmentioning

confidence: 99%

A Synergistic Transcriptional Regulation of Olfactory Genes Drives Blood-Feeding Associated Complex Behavioral Responses in the Mosquito Anopheles culicifacies

Thomas

Verma

et al. 2018

Front. Physiol.

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“…aegypti is a major arbovirus vector and thus a primary target of control efforts, including those involving the release of genetically modified mosquitoes [ 111 ]. Recent work in mosquitoes has uncovered common biological drivers behind mating, host-seeking, and blood-feeding behaviors [ 112 ]. Future research into female post-mating responses related to interconnected, epidemiologically impactful behaviors such as blood feeding will undoubtedly provide important biological insights that can be leveraged to create more effective vector and disease control strategies.…”

Section: Discussionmentioning

confidence: 99%

The impact of mating and sugar feeding on blood-feeding physiology and behavior in the arbovirus vector mosquito Aedes aegypti

et al. 2021

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Background Aedes aegypti mosquitoes are globally distributed vectors of viruses that impact the health of hundreds of millions of people annually. Mating and blood feeding represent fundamental aspects of mosquito life history that carry important implications for vectorial capacity and for control strategies. Females transmit pathogens to vertebrate hosts and obtain essential nutrients for eggs during blood feeding. Further, because host-seeking Ae. aegypti females mate with males swarming near hosts, biological crosstalk between these behaviors could be important. Although mating influences nutritional intake in other insects, prior studies examining mating effects on mosquito blood feeding have yielded conflicting results. Methodology/Principal findings To resolve these discrepancies, we examined blood-feeding physiology and behavior in virgin and mated females and in virgins injected with male accessory gland extracts (MAG), which induce post-mating changes in female behavior. We controlled adult nutritional status prior to blood feeding by using water- and sugar-fed controls. Our data show that neither mating nor injection with MAG affect Ae. aegypti blood intake, digestion, or feeding avidity for an initial blood meal. However, sugar feeding, a common supplement in laboratory settings but relatively rare in nature, significantly affected all aspects of feeding and may have contributed to conflicting results among previous studies. Further, mating, MAG injection, and sugar intake induced declines in subsequent feedings after an initial blood meal, correlating with egg production and laying. Taking our evaluation to the field, virgin and mated mosquitoes collected in Colombia were equally likely to contain blood at the time of collection. Conclusions/Significance Mating, MAG, and sugar feeding impact a mosquito’s estimated ability to transmit pathogens through both direct and indirect effects on multiple aspects of mosquito biology. Our results highlight the need to consider natural mosquito ecology, including diet, when assessing their physiology and behavior in the laboratory.

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“…culicifacies. In contrast to the pre-blood meal olfactory responses, which are signi cantly in uenced by age/sex/circadian even in the absence of host-exposure (De et al 2017(De et al , 2018b;…”

Section: Gut-metabolic Switch Modulates the Brain's Energy Metabolism And Functional Engagementmentioning

confidence: 95%

“…We recently demonstrated that both mating and circadian rhythm have an important role in driving olfactory guided pre-blood-mealassociated behavioral properties in the aging adult female mosquito An. culicifacies (De et al 2017(De et al , 2018bDas De et al 2018). Aligning to olfactory responses, here, we aimed to decode and establish a possible molecular correlation between brain and gut-metabolic switch, and desgined a similar RNA-Seq strategy (Fig.…”

Section: Hypothesismentioning

confidence: 99%

“…Recently, we have demonstrated that prior host-exposure sex, and circadian have a signi cant impact on the olfactory responses in the aging adult-female An. culicifacies mosquito (De et al 2017(De et al , 2018b; Das De et al 2018). Likewise, to test and evaluate the possible correlation of age with neuroregulation, we monitored the expression pro le of at least 14 neuro-modulatory genes in aging naïve adult female mosquito's brain (Fig.…”

Section: Spatial and Temporal Modulations Of Neuro-signaling In Uences Metabolic Switch-associated Physiological Activitiesmentioning

confidence: 99%

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Microbiome-Gut-Brain-Axis Communication Influences Metabolic Switch in the Mosquito Anopheles Culicifacies

Dixit

2021

Preprint

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Periodic ingestion of a protein-rich blood meal by adult female mosquitoes causes a drastic metabolic change in their innate physiological status, which is referred to as ‘metabolic switch. Although the down-regulation of olfactory factors is key to restrain host-attraction, how the gut ‘metabolic switch’ modulates brain functions, and resilience physiological homeostasis remains unexplored. Here we demonstrate that the protein-rich diet induces the expression of brain transcripts related to mitochondrial function and energy metabolism, possibly to cause a shift of the brain’s engagement to manage organismal homeostasis. A dynamic expression pattern of neuro-signalling and neuro-modulatory genes in both gut and brain, establishes an active brain-distant organ communication. Disruption of this comunication through decapitation, does not affect the modulation of the neuro-modulator receptor genes in the gut. In parallel, an unusual and paramount shift in the level of the Neurotransmitters (NTs), from the brain to the gut after blood feeding, further supports the idea of the gut’s ability to serve as a ‘second brain’. Finally, a comparative metagenomics evaluation of gut microbiome population dynamics, highlighted that blood-feeding not only suppresses Enterobacteriaceae family member by 50%, but favors rapid proliferation of Pseudomonadales to 46% of the total community. Notable obesrvation of a rapid proliferation of Pseudomonas bacterial sp. in the gut correlates a possible cause for the suppression of appetite after blood-feeding. Additionally, an altered NTs dynamics of naïve and aseptic mosquitoes provide the initial evidence that gut-endosymbionts are key modulators for the synthesis of major neuroactive molecules. Conclusion: Our data establish a new conceptual understanding of microbiome-gut-brain-axis communication in mosquitoes.Data deposition: Mosquito Brain RNAseq data are accessible under Accession IDs: SRR9853884 (Ac-Br-SF); SRR9853885 (Ac-Br-BF-30Min), SRR9853883 (Ac-Br-BF-30hrs) at NCBI repository. Mosquito Gut metagenomics data are accessible under accession IDs: SRR12579422 (Ac-MG-SF); SRR12622557 (Ac-MG-BF) at NCBI repository.

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Sex specific molecular responses of quick-to-court protein in Indian malarial vector Anopheles culicifacies : conflict of mating versus blood feeding behaviour

Cited by 9 publications

References 35 publications

A Synergistic Transcriptional Regulation of Olfactory Genes Drives Blood-Feeding Associated Complex Behavioral Responses in the Mosquito Anopheles culicifacies

A Synergistic Transcriptional Regulation of Olfactory Genes Drives Blood-Feeding Associated Complex Behavioral Responses in the Mosquito Anopheles culicifacies

The impact of mating and sugar feeding on blood-feeding physiology and behavior in the arbovirus vector mosquito Aedes aegypti

Microbiome-Gut-Brain-Axis Communication Influences Metabolic Switch in the Mosquito Anopheles Culicifacies

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