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UNIVERSITY of CALIFORNIA RIVERSIDE Gustatory Receptors In UNIVERSITY OF CALIFORNIA RIVERSIDE Gustatory Receptors in Mosquito Olfaction and Host-Seeking Behavior A Dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Entomology by Genevieve Mitchell Tauxe March 2015 Dissertation Committee: Dr. Anandasankar Ray, Chairperson Dr. Michael E. Adams Dr. Ring T. Cardé Dr. Jocelyn G. Millar Copyright by Genevieve Mitchell Tauxe 2015 The Dissertation of Genevieve Mitchell Tauxe is approved: Committee Chairperson University of California, Riverside Acknowledgements First, I thank the anonymous odor donors who participated in the experiments described here. They variously washed their feet in the bathroom sink, walked around for hours with beads in their socks (which, no, is not terribly comfortable), and continually showed up no matter how many times we kept asking for more socks. Thank you for your generosity, and for your stinky feet. Now go find yourself on page 73. I thank my advisor, Anand Ray, for all of his help and support over my graduate career. He has taught me so much about how to do research, and also how to compose manuscripts, give presentations, and talk about science. I also thank my committee members, Ring Cardé, Jocelyn Millar, and Mike Adams, for offering so much helpful advice and support over the years, both during official committee meetings and on many other occasions. I thank all the Ray lab and Dahanukar lab members for making the laboratory a fun and productive place to work. In particular, Paulina Ngo performed most of the behavior tests reported in Chapter 4, Tom Guda helped with many behavioral assays, and Greg Pask helped with cloning. I also thank Anupama Dahanukar and Marco Metzger for useful discussions. Finally, to all of my family and friends, near and far, who have stuck by me during this whole process—you who fed me, kept me company, told me to get back to work when I needed to hear it, or to take a break when I needed that: Thank you. Your support has turned the impossible into the real. iv Funding for the work described in this dissertation was provided by a grant to A Ray from the NIH (NIAID) grant to A. Ray, award number R01AI087785. Additional support was provided to GMT by the Chancellor’s Distinguished Fellowship (UCR), the OneHealth Summer Research Fellowship (University of California Global Health Institute and the Bill and Melinda Gates Foundation), and from the Dr. Janet M. Boyce Memorial Endowed Fund for Women Majoring in the Sciences (UCR College of Natural and Agricultural Sciences). The text of this dissertation, in part, is a reprint of material as it appears in the paper “Targeting a dual detector of skin and CO2 to modify mosquito host seeking” (Cell 155:1365-1379). In particular, material from that publication is included throughout Chapter 2 and in Fig. 4.2. The co-authors Dyan MacWilliam, Sean Boyle, and Tom Guda listed in that publication contributed original research to the publication that is not included in this dissertation. The co-author Anandasankar Ray listed in that publication directed and supervised the research that forms the basis for this dissertation. v ABSTRACT OF THE DISSERTATION Gustatory Receptors in Mosquito Olfaction and Host-Seeking Behavior by Genevieve Mitchell Tauxe Doctor of Philosophy, Graduate Program in Entomology University of California, Riverside, March 2015 Dr. Anandasankar Ray, Chairperson Female mosquitoes have evolved multiple strategies to find hosts from a distance by their odor. Few compounds from the human odor blend are known to mediate these behaviors. One is carbon dioxide (CO2), which activates resting mosquitoes and triggers upwind flight. CpA neurons on the maxillary palps express three members of the gustatory receptor (GR) family and detect CO2. I found that CO2-sensitive cpA neurons in both Aedes aegypti and Anopheles gambiae also detect components of the human odor blend. CpA responses to these odorants closely resemble its responses to CO2, and when CO2 and skin odorants are presented together, cpA responds more strongly to the combination than to either alone. CpA also detects the natural human odor blend. A novel long-term inhibitor of cpA was used to block cpA activity, and behavioral tests in cpA–off mosquitoes revealed specific deficits in behavioral activation in response to odor, even without a CO2 stimulus. vi Genes for the receptor subunits Gr1, 2, and 3 were cloned and expressed in the Drosophila ab1C neuron. In mutants lacking Drosophila receptors, Gr2 and Gr3 form a functional receptor that is as sensitive to CO2 and more sensitive to other odorants than when Gr1 is added. Two inhibitors reduced CO2 responses in neurons expressing Gr2+3, and adding Gr1 modulated their activity in an odorant-specific manner. When mosquito GRs are expressed with Drosophila GRs, they form a CO2 receptor only when both mosquito Gr1+2 and Drosophila Gr63a are present, providing clues to the evolutionary history of protein interactions in this receptor class. Mosquitoes use odor to discriminate between more and less preferred hosts. Human participants were ranked in attractiveness in wild type and mutant mosquitoes lacking function in cpA or other olfactory neurons. Mutants had altered preferences from wild type. Additional studies may elucidate the mechanisms by which these receptors contribute to preference. The results of this study integrate molecular, physiological, and behavioral experiments to decode more of the links between a mosquito’s chemical environment and her behavioral output. Better understanding the mechanisms driving host-seeking behavior will contribute to critically needed new strategies for combating mosquito-borne disease. vii Table of Contents Chapter 1. Mosquito olfaction and host-seeking behavior. ............................................... 1 Model species for host-seeking behavior ............................................................ 2 Composition and origins of human odor ............................................................ 3 Organization of the mosquito olfactory system .................................................. 5 A minimal stimulus induces host-seeking behavior ........................................... 8 Activation ............................................................................................................ 8 Anemotaxis ....................................................................................................... 11 Landing ............................................................................................................. 13 Trap Catch ......................................................................................................... 14 Preference ......................................................................................................... 19 Current progress and challenges ....................................................................... 22 Chapter 2. A single olfactory neuron class mediates mosquito activation by both carbon dioxide and skin odor ........................................................................................................ 25 The CO2-sensitive cpA neuron also detects human odorants ........................... 28 Two human-associated odorants are inhibitors of cpA..................................... 34 CpA detects whole human odor ........................................................................ 35 Butyryl chloride is a long-term inhibitor of cpA .............................................. 37 CpA is required for behavioral activation by human odor ............................... 45 viii Discussion ......................................................................................................... 50 Methods............................................................................................................. 52 Mosquitoes ........................................................................................................ 52 Odors and stimulus presentation ....................................................................... 53 Electrophysiology ............................................................................................. 55 Chemical genetics ............................................................................................. 57 Behavior ............................................................................................................ 57 Statistics ............................................................................................................ 59 Ethics................................................................................................................. 59 Chapter 3. Functional analysis of subunit interactions in the insect carbon dioxide receptor. ............................................................................................................................ 60 The cloned gustatory receptor genes AaGr1, Gr2, and Gr3 ............................. 63 The empty neuron system ................................................................................. 65 Fine tuning the ab1C empty neuron system ...................................................... 69 Inhibition of the transgenic ab1C neuron.......................................................... 71 Co-expressed mosquito and Drosophila receptors interact .............................. 72 Discussion ......................................................................................................... 78 Methods............................................................................................................
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