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Molecular characterization of the carbon dioxide receptor in the oriental latrine fly, Chrysomya megacephala (Diptera: Calliphoridae)

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Abstract

The blowfly Chrysomya megacephala (Fabricius) (Diptera: Calliphoridae) cannot only act as a mechanical vector of various pathogens, but also infest man and animals causing human health problems and economic losses in the livestock and fish industries. As in other insects, olfaction of this species plays an important role in host location and is presumably mediated via transmembrane receptor signaling pathways. Here, we isolate and characterize CmegGr1 and CmegGr2, two new members of the chemosensory receptor gene family from C. megacephala. The open reading frames of CmegGr1 and CmegGr2 cDNA clones encode 453 and 486 amino acid residues, respectively. These two deduced proteins display high amino acid conservation with previously identified carbon dioxide (CO2) receptors, such as Drosophila melanogaster Gr21a/Gr63a and Anopheles gambiae s.s. Gr22/Gr24. Further sequence analysis showed that both proteins are consistent with their corresponding orthologs in the membrane topology prediction with some ambiguities in the location of N terminus and the number of transmembrane domains. The transcripts of CmegGr1 and CmegGr2 were detected in the major chemosensory organs including the antennae and proboscises with maxillary palps attached. These results suggest that CmegGr1 and CmegGr2 are likely to be the primary receptors for CO2 detection in C. megacephala. Knowledge of the molecular identity of the blowfly olfactory CO2 receptors may aid in the development of novel control strategies designed to take advantage of this unique and critical olfactory pathway.

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References

  • Barton Browne L (1960) The role of olfaction in the stimulation of oviposition in the blowfly, Phormia regina. J Insect Physiol 5:16–22

    Article  Google Scholar 

  • Benton R, Sachse S, Michnick SW, Vosshall LB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4:e20

    Article  PubMed  Google Scholar 

  • Boto T, Gomez-Diaz C, Alcorta E (2010) Expression analysis of the 3G-protein subunits, Galpha, Gbeta, and Ggamma, in the olfactory receptor organs of adult Drosophila melanogaster. Chem Senses 35:183–193

    Article  PubMed  CAS  Google Scholar 

  • Bowen MF (1991) The sensory physiology of host-seeking behavior in mosquitoes. Annu Rev Entomol 36:139–158

    Article  PubMed  CAS  Google Scholar 

  • Clyne PJ, Warr CG, Carlson JR (2000) Candidate taste receptors in Drosophila. Science 287:1830–1834

    Article  PubMed  CAS  Google Scholar 

  • de Bruyne M, Foster K, Carlson JR (2001) Odor coding in the Drosophila antenna. Neuron 30:537–552

    Article  PubMed  Google Scholar 

  • Dunipace L, Meister S, McNealy C, Amrein H (2001) Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr Biol 11:822–835

    Article  PubMed  CAS  Google Scholar 

  • Esser JR (1991) Biology of Chrysomya megacephala (Diptera: Calliphoridae) and reduction of losses caused to the salted-dried fish industry in south-east Asia. Bull Entomol Res 81:33–42

    Article  Google Scholar 

  • Faucher C, Forstreuter M, Hilker M, de Bruyne M (2006) Behavioral responses of Drosophila to biogenic levels of carbon dioxide depend on life-stage, sex and olfactory context. J Exp Biol 209:2739–2748

    Article  PubMed  CAS  Google Scholar 

  • Fischler W, Kong P, Marella S, Scott K (2007) The detection of carbonation by the Drosophila gustatory system. Nature 448:1054–1057

    Article  PubMed  CAS  Google Scholar 

  • Gibson G, Torr SJ (1999) Visual and olfactory responses of haematophagous Diptera to host stimuli. Med Vet Entomol 13:2–23

    Article  PubMed  CAS  Google Scholar 

  • Greenberg B (1973) Flies and disease. Vol. 2. Biology and disease transmission, vol 2. Princeton University Press, Princeton

    Google Scholar 

  • Guerenstein PG, Hildebrand JG (2008) Roles and effects of environmental carbon dioxide in insect life. Annu Rev Entomol 53:161–178

    Article  PubMed  CAS  Google Scholar 

  • Jones WD, Cayirlioglu P, Kadow IG, Vosshall LB (2007) Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445:86–90

    Article  PubMed  CAS  Google Scholar 

  • Kent LB, Walden KK, Robertson HM (2008) The Gr family of candidate gustatory and olfactory receptors in the yellow-fever mosquito Aedes aegypti. Chem Senses 33:79–93

    Article  PubMed  CAS  Google Scholar 

  • Kleineidam C, Roces F (2000) Carbon dioxide concentrations and nest ventilation in nests of the leaf-cutting ant Atta vollenweideri. Insectes Soc 47:241–248

    Article  Google Scholar 

  • Kumarasinghe SP, Karunaweera ND, Ihalamulla RL (2000) A study of cutaneous myiasis in Sri Lanka. Int J Dermatol 39:689–694

    Article  PubMed  CAS  Google Scholar 

  • Kwon JY, Dahanukar A, Weiss LA, Carlson JR (2007) The molecular basis of CO2 reception in Drosophila. Proc Natl Acad Sci U S A 104:3574–3578

    Article  PubMed  CAS  Google Scholar 

  • Laissue PP, Vosshall LB (2008) The olfactory sensory map in Drosophila. Adv Exp Med Biol 628:102–114

    Article  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43:703–714

    Article  PubMed  CAS  Google Scholar 

  • LéBlanc HN, Logan JG (2010) Exploiting insect olfaction in forensic entomology. In: Amendt J, Goff ML, Campobasso CP, Grassberger M (eds) Current concepts in forensic entomology. Springer, New York, pp 205–221

    Google Scholar 

  • Lu T, Qiu YT, Wang G, Kwon JY, Rutzler M, Kwon HW, Pitts RJ, van Loon JJ, Takken W, Carlson JR, Zwiebel LJ (2007) Odor coding in the maxillary palp of the malaria vector mosquito Anopheles gambiae. Curr Biol 17:1533–1544

    Article  PubMed  CAS  Google Scholar 

  • Lundin C, Kall L, Kreher SA, Kapp K, Sonnhammer EL, Carlson JR, Heijne G, Nilsson I (2007) Membrane topology of the Drosophila OR83b odorant receptor. FEBS Lett 581:5601–5604

    Article  PubMed  CAS  Google Scholar 

  • Luo M, Sun L, Hu J (2009) Neural detection of gases—carbon dioxide, oxygen—in vertebrates and invertebrates. Curr Opin Neurobiol 19:354–361

    Article  PubMed  CAS  Google Scholar 

  • Malpel S, Merlin C, Francois MC, Jacquin-Joly E (2008) Molecular identification and characterization of two new Lepidoptera chemoreceptors belonging to the Drosophila melanogaster OR83b family. Insect Mol Biol 17:587–596

    Article  PubMed  CAS  Google Scholar 

  • Mehlhorn H (2008) Encyclopedia of parasitology, 3rd edn. Springer, New York

    Book  Google Scholar 

  • Meyerhof W, Korsching S (2009) Chemosensory systems in mammals, fishes, and insects. Springer, Heidelberg

    Google Scholar 

  • Murugan K, Kovendan K, Vincent S, Barnard DR (2012) Biolarvicidal and pupicidal activity of Acalypha alnifolia Klein ex Willd. (Family: Euphorbiaceae) leaf extract and microbial insecticide, Metarhizium anisopliae (Metsch.) against malaria fever mosquito, Anopheles stephensi Liston. (Diptera: Culicidae). Parasitol Res 110:2263–2270

    Article  PubMed  Google Scholar 

  • Nakagawa T, Vosshall LB (2009) Controversy and consensus: noncanonical signaling mechanisms in the insect olfactory system. Curr Opin Neurobiol 19:284–292

    Article  PubMed  CAS  Google Scholar 

  • Ngoen-klan R, Moophayak K, Klong-klaew T, Irvine KN, Sukontason KL, Prangkio C, Somboon P, Sukontason K (2011) Do climatic and physical factors affect populations of the blow fly Chrysomya megacephala and house fly Musca domestica? Parasitol Res 109:1279–1292

    Article  PubMed  Google Scholar 

  • Robertson HM, Kent LB (2009) Evolution of the gene lineage encoding the carbon dioxide receptor in insects. J Insect Sci 9:19

    PubMed  Google Scholar 

  • Robertson HM, Warr CG, Carlson JR (2003) Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci U S A 100(Suppl 2):14537–14542

    Article  PubMed  CAS  Google Scholar 

  • Sato K, Pellegrino M, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452:1002–1006

    Article  PubMed  CAS  Google Scholar 

  • Sato K, Tanaka K, Touhara K (2011) Sugar-regulated cation channel formed by an insect gustatory receptor. Proc Natl Acad Sci U S A 108:11680–11685

    Article  PubMed  CAS  Google Scholar 

  • Scott K, Brady R Jr, Cravchik A, Morozov P, Rzhetsky A, Zuker C, Axel R (2001) A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104:661–673

    Article  PubMed  CAS  Google Scholar 

  • Smart R, Kiely A, Beale M, Vargas E, Carraher C, Kralicek AV, Christie DL, Chen C, Newcomb RD, Warr CG (2008) Drosophila odorant receptors are novel seven transmembrane domain proteins that can signal independently of heterotrimeric G proteins. Insect Biochem Mol Biol 38:770–780

    Article  PubMed  CAS  Google Scholar 

  • Sonnhammer EL, Wootton JC (2001) Integrated graphical analysis of protein sequence features predicted from sequence composition. Proteins 45:262–273

    Article  PubMed  CAS  Google Scholar 

  • Southwick EE, Moritz RFA (1987) Social control of air ventilation in colonies of honey bees, Apis mellifera. J Insect Physiol 33:623–626

    Article  Google Scholar 

  • Stange G (1997) Effects of changes in atmospheric carbon dioxide on the location of hosts by the moth, Cactoblastis cactorum. Oecologia 110:539–545

    Article  Google Scholar 

  • Stange G, Stowe S (1999) Carbon-dioxide sensing structures in terrestrial arthropods. Microsc Res Tech 47:416–427

    Article  PubMed  CAS  Google Scholar 

  • Sugahara M, Sakamoto F (2009) Heat and carbon dioxide generated by honeybees jointly act to kill hornets. Naturwissenschaften 96:1133–1136

    Article  PubMed  CAS  Google Scholar 

  • Suh GS, Wong AM, Hergarden AC, Wang JW, Simon AF, Benzer S, Axel R, Anderson DJ (2004) A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431:854–859

    Article  PubMed  CAS  Google Scholar 

  • Sukontason K, Sukontason KL, Piangjai S, Boonchu N, Chaiwong T, Ngern-Klun R, Sripakdee D, Vogtsberger RC, Olson JK (2004) Antennal sensilla of some forensically important flies in families Calliphoridae, Sarcophagidae and Muscidae. Micron 35:671–679

    Article  PubMed  Google Scholar 

  • Sukontason KL, Bunchoo M, Khantawa B, Piangjai S, Rongsriyam Y, Sukontason K (2007) Comparison between Musca domestica and Chrysomya megacephala as carriers of bacteria in northern Thailand. Southeast Asian J Trop Med Public Health 38:38–44

    PubMed  Google Scholar 

  • Sukontason KL, Narongchai P, Sripakdee D, Boonchu N, Chaiwong T, Ngern-Klun R, Piangjai S, Sukontason K (2005) First report of human myiasis caused by Chrysomya megacephala and Chrysomya rufifacies (Diptera: Calliphoridae) in Thailand, and its implication in forensic entomology. J Med Entomol 42:702–704

    Article  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • Thom C, Guerenstein PG, Mechaber WL, Hildebrand JG (2004) Floral CO2 reveals flower profitability to moths. J Chem Ecol 30:1285–1288

    Article  PubMed  CAS  Google Scholar 

  • Tsitoura P, Andronopoulou E, Tsikou D, Agalou A, Papakonstantinou MP, Kotzia GA, Labropoulou V, Swevers L, Georgoussi Z, Iatrou K (2010) Expression and membrane topology of Anopheles gambiae odorant receptors in lepidopteran insect cells. PLoS One 5:e15428

    Article  PubMed  CAS  Google Scholar 

  • Turner SL, Ray A (2009) Modification of CO2 avoidance behaviour in Drosophila by inhibitory odorants. Nature 461:277–281

    Article  PubMed  CAS  Google Scholar 

  • Vosshall LB, Hansson BS (2011) A unified nomenclature system for the insect olfactory coreceptor. Chem Senses 36:497–498

    Article  PubMed  Google Scholar 

  • Wall R, Howard JJ, Bindu J (2001) The seasonal abundance of blowflies infesting drying fish in south-west India. J Appl Ecol 38:339–348

    Article  Google Scholar 

  • Wall R, Shearer D (2001) Veterinary ectoparasites: biology, pathology and control, 2nd edn. Blackwell Science, Oxford

    Book  Google Scholar 

  • Wall R, Warnes M (1994) Responses of the sheep blowfly Lucilia sericata to carrion odour and carbon dioxide. Entomol Exp Appl 73:239–246

    Article  Google Scholar 

  • Wang X, Zhong M, Wen J, Cai J, Jiang H, Liu Y, Aly SM, Xiong F (2012) Molecular characterization and expression pattern of an odorant receptor from the myiasis-causing blowfly, Lucilia sericata (Diptera: Calliphoridae). Parasitol Res 110:843–851

    Article  PubMed  Google Scholar 

  • Wanner KW, Robertson HM (2008) The gustatory receptor family in the silkworm moth Bombyx mori is characterized by a large expansion of a single lineage of putative bitter receptors. Insect Mol Biol 17:621–629

    Article  PubMed  CAS  Google Scholar 

  • Wells JD (1991) Chrysomya megacephala (Diptera: Calliphoridae) has reached the continental United States: review of its biology, pest status, and spread around the world. J Med Entomol 28:471–473

    PubMed  CAS  Google Scholar 

  • Wicher D, Schafer R, Bauernfeind R, Stensmyr MC, Heller R, Heinemann SH, Hansson BS (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452:1007–1011

    Article  PubMed  CAS  Google Scholar 

  • Xia H, Li G, Ma X (2010) Laboratory study on azadirachtin to protect salted sun-dried fish from chrysomya megacephala infestation. J Food Process Preserv 34:35–54

    Article  Google Scholar 

  • Yao CA, Carlson JR (2010) Role of G-proteins in odor-sensing and CO2-sensing neurons in Drosophila. J Neurosci 30:4562–4572

    Article  PubMed  CAS  Google Scholar 

  • Zhang D, Wang QK, Hu DF, Li K (2012) Cuticular structures on antennae of the bot fly, Portschinskia magnifica (Diptera: Oestridae). Parasitol Res 111:1651–1659

    Article  PubMed  Google Scholar 

  • Zhang HJ, Anderson AR, Trowell SC, Luo AR, Xiang ZH, Xia QY (2011) Topological and functional characterization of an insect gustatory receptor. PLoS One 6:e24111

    Article  PubMed  CAS  Google Scholar 

  • Zumpt F (1965) Myiasis in man and animals in the Old World. Butterworths, London

    Google Scholar 

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Acknowledgments

This work was supported by Hunan Provincial Innovation Foundation for Postgraduate (CX2010B037, CX2010B038).

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Pathology, Central South University, Changsha, 410013, Hunan, China

    Xiang Wang, Ming Zhong, Qinlai Liu, Chang Wu & Jifang Wen

  2. Department of Forensic Medicine, Faculty of Medicine, Suez Canal University, Ismailia, 41522, Egypt

    Sanaa Mohamed Aly

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  1. Xiang Wang
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  2. Ming Zhong
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  3. Qinlai Liu
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  4. Sanaa Mohamed Aly
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  5. Chang Wu
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Correspondence to Jifang Wen.

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Wang, X., Zhong, M., Liu, Q. et al. Molecular characterization of the carbon dioxide receptor in the oriental latrine fly, Chrysomya megacephala (Diptera: Calliphoridae). Parasitol Res 112, 2763–2771 (2013). https://doi.org/10.1007/s00436-013-3410-7

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  • DOI: https://doi.org/10.1007/s00436-013-3410-7

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