The Taste of Blood in Mosquitoes
Posted on: 23 April 2020
Preprint posted on 27 February 2020
Article now published in Neuron at http://dx.doi.org/10.1016/j.neuron.2020.09.019
I’ll have a blood meal to go–no milk, no sugar: Female Aedes aegypti mosquito stylet neurons drive discrimination between blood and nectar based on neuronal activation by blood components
Selected by Vaibhav Menon
Categories: animal behavior and cognition, evolutionary biology, genetics, neuroscience
Background
Aedes aegypti is is a species of mosquito that is a particularly effective vector for viruses that cause diseases including yellow fever, dengue fever, chikungunya fever, and Zika fever [1]. These diseases are transmitted when the female mosquito bites humans in search of a blood meal. This preference for a blood-meal, however, is context-dependent. Sugar from nectar provides an energy source for the insect, but to progress egg development, mated female mosquitoes require blood. Additionally, the anatomical program by which a mosquito feeds on blood has been demonstrated to be distinct from its sugar-feeding tract. Nectar, a sugar-rich food source present in flowers, is sensed by the labium whereas blood is consumed by the sharp needle-like labrum organ, also known as the stylet. While previous studies have shown that the blood-feeding behavior can be observed in the context of human cues such as CO2 plumes or heat, it is not clear how blood specifically is sensed before consumption [2]. In this preprint, the authors comprehensively demonstrate the sexually dimorphic expression of gustatory receptor neurons (GRNs) on the stylet that poise the female to respond uniquely to the components of blood, including glucose, NaHCO3, NaCl, and ATP. In doing so, they clearly illustrate that blood sensing is a complex integration of multiple, distinct taste qualities mediated by at least two classes of ionotropic receptors (Irs).
Key findings:
Blood-sensing and sugar-sensing are separable behaviors
Feeding assays demonstrated that the volume of blood consumed by the female mosquito was triple that of sucrose-consumption. Blood localized to the midgut after consumption, whereas sucrose localized to the crop. These observations pointed to a difference in behavioral programs driving blood-feeding and nectar-feeding. In Drosophila melanogaster, Gr5aand Gr64f are established sugar-sensing neurons. The closest ortholog to these in mosquitos is Gr4. Thus, the authors used CRISPR-Cas9 genome editing to insert the binary expression construct QF2 at the Gr4 locus to gain genetic access to this potential sweet-tasting neuron. Indeed, they confirmed its role in responding to sugar by chemogenetically activating this population and observing feeding behavior responses to water comparable to those of sucrose. So how does blood-sensing fit in?
To probe at the evaluation of blood prior to consumption, the authors noted that in the presence of human cues CO2 and heat, females would reliably feed to engorgement on blood and an ATP/saline solution, but not sucrose or saline alone. The presence of human cues, in other words, is followed by a separate evaluation of the food source that allows for selection of blood or blood components over sugar.
Neural expression and projection patterns are sex-specific and organ-specific, respectively
Examination of the stylet under pan-neuronal GCaMP expression, nuclear and dendritic staining reveal significantly more cell bodies and dendritic processes in the female stylet than the male stylet. Dye-fill experiments comparing stylet neurons to labium neurons illustrate a non-overlapping projection region to the subesophageal zone (the first projection of taste information in insects) from the two organs.
Mosquito behavior and stylet neuron activity in response to blood can be broken down component-wise
GCaMP6s responses to repeated presentations of blood showed non-adapting, robust calcium signals in a significant number of stylet neurons. Water failed to elicit such a response. Using a combination of 4 components of blood that have shown to increase likelihood of engorgement–ATP, glucose, NaHCO3, NaCl–the authors observed calcium responses similar to that of blood. Observation of responses to these components individually demonstrated the component-wise stylet response. Neurons could be clustered based on the component they responded most robustly to, creating groups of neurons that responded uniquely to ATP, NaHCO3, NaCl, a population that responded to all 3, and a population that did not respond to any of these. Through this experiment, the authors suggest that the blood response can understood as an integration of information from different taste modalities.
Blood-sensing neurons localized to stylet, sugar sensing neurons localized to labium
The authors then analyzed RNA-seq data of stylet tissue to identify significantly enriched genes in the female stylet and labium. They identified two ionotropic receptors, Ir7a and Ir7f, that were unique to the female stylet. After gaining binary expression control and genetic access of these neurons, functional imaging using the 4 components of blood revealed Ir7a responses were most robust in the presence of NaHCO3. Ir7f neurons, on the other hand, responded most robustly to the mix of all 4 components. These neurons reflected the response profile of the integrator cluster of neurons identified in pan-neuronal GCaMP6s expression experiments of the stylet. RNA-seq expression analysis further revealed expression in the labium but notably not the stylet of orthologs of known sugar receptors in D. melanogaster, suggesting that blood-sensing and sugar-sensing behaviors are also distinct in the neuronal organization that governs each program.
Why I liked this paper:
This paper was an exhaustive study of a previously understudied organ of the mosquito. Given the role blood-feeding has on the proliferation of deadly diseases that debilitate millions, this study also struck me as a compelling and important undertaking. I chose this paper because I am interested in gustatory behavior and integration of sensory information associated with feeding. Mosquitos demonstrate two totally different feeding behaviors, so a model incorporating segregation of taste organs and thus neuronal input would be a simple, yet elegant explanation for how these behaviors diverge. At a minimum, this thorough characterization of the stylet provides a critical foundation for which blood-feeding and behavior can be further explored.
Future Directions:
- Given the stylet’s unique role in blood-feeding, what information do you think the population of neurons that failed to respond to blood may be sensing? You mentioned potential thermosensory or mechanosensory roles. If these neurons were mechanosensory, I would have expected to see them activate during feeding anyway.
- The labrum is one of the mouthparts of the mosquito that are involved in processes of feeding. While the labrum is the mouthpart that pierces skin, are the other mouthparts receiving input from the periphery that might influence blood-feeding?
References
1.Powell JR. Mosquito-Borne Human Viral Diseases: Why Aedes aegypti?. Am J Trop Med Hyg. 2018;98(6):1563–1565. doi:10.4269/ajtmh.17-0866
2. McMeniman, C.J., Corfas, R.A., Matthews, B.J., Ritchie, S.A., and Vosshall, L.B. (2014). Multimodal integration of carbon dioxide and other sensory cues drives mosquito attraction to humans. Cell 156, 1060-1071.
doi: https://doi.org/10.1242/prelights.19179
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