Abstract
The endosymbiotic bacterium Wolbachia infects various insects and is primarily known for its ability to manipulate host reproduction. Recent investigations reveal that Wolbachia also affects the activity of somatic cells. We here demonstrated by trap method and T-maze that Wolbachia infection had significant impact on the olfactory response of Drosophila simulans. Wolbachia-infected flies took shorter time to enter the food trap and were more sensitive to odorant in T-maze than those uninfected controls. The time of olfactory response was relative to Wolbachia density in flies. Wolbachia density in 15-day-old flies that were caught in a shorter time (less than 60 min) by food trap was significantly higher than those taken in a longer time (more than 100 min). Quantitative RT-PCR showed that the transcript of an important odorant receptor gene or83b in flies with fast olfactory response was significantly more than those with slow olfactory response. These results suggest that Wolbachia might increase olfactory response of flies by regulating the expression of olfaction-related genes in hosts.
References
Werren J H, Windsor D M, Guo L R. Distribution of Wolbachia among neotropical arthropods. Proc R Soc Lond B, 1995, 262: 197–204
Rowley S M, Raven R J, McGraw E A. Wolbachia pipientis in Australian spiders. Curr Microbiol, 2004, 49(3): 208–214
Werren J H. Biology of Wolbachia. Annu Rev Entomol, 1997, 42: 587–609
McGraw E A, O’Neill S L. Wolbachia pipientis: Intracellular infection and pathogenesis in Drosophila. Curr Opin Microbiol, 2004, 7(1): 67–70
Mouton L, Dedeine F, Henri H, et al. Virulence, multiple infections and regulation of symbiotic population in the Wolbachia-Asobara tabida symbiosis. Genetics, 2004, 168(1): 181–189
McGraw E A, Merritt D J, Droller J N, et al. 2002. Wolbachia density and virulence attenuation following transfer into a novel host. Proc Natl Acad Sci USA, 2002, 99(5): 2918–2923
Reynolds K T, Thomson L J, Hoffmann A A. The effects of host age, host nucleus background and temperature on phenotypic effects of the virulent Wolbachia strain popcorn in Drosophila melanogaster. Genetics, 2003, 164(3): 1027–1034
Fry A J, Palmer M R, Rand D M. Variable fitness effects of Wolbachia infection in Drosophila melanogaster. Heredity, 2004, 93(4): 379–389
Hansson B S. A bug’s smell-research into insect olfaction. Trends Neurosci, 2002, 25(5): 270–274
Gibson G, Torr S J. Visual and olfactory responses of haematophagus Diptera to host stimuli. Med Veter Entomol, 1999, 13(1): 2–23
Charlton R E, Kanno H, Collins R D, et al. Influence of pheromone concentration and ambient temperature on flight of the gypsy moth, Lymantria dispar (L.), in a sustained-flight wind tunnel. Physiol Entomol, 1993, 18: 349–362
Hoffmann A A, Turelli M. Distribution of Drosophila melanogaster on alternative resources: Effects of experience and starvation. Am Nat, 1985, 126: 662–679
Barron A B, Corbet S A. Pre-exposure affects the olfactory response of Drosophila melanogaster to menthol. Entomol Exp Appl, 1999, 90: 175–181
Devaud J M. Experimental studies of adult Drosophila chemosensory behaviour. Behav Proc, 2003, 64(2): 177–196
Dudai Y D, Jan Y N, Byers D C, et al. dunce, a mutant of Drosophila deficient in learning. Proc Natl Acad Sci USA, 1976, 73: 1684–1688
Wang Y L, Chiang A S, Xia S Z, et al. Blockade of neurotransmission in Drosophila mushroom bodies impairs odor attraction, but not repulsion. Curr Biol, 2003, 13: 1900–1904
Zhou X J, Yuan C Y, Guo A K. Drosophila olfactory response rhythms require clock genes but not pigment dispersing factor lateral neurons. J Biol Rhythms, 2005, 20: 237–244
McGraw E A, Merritt D J, Droller J N, et al. Wolbachia mediated sperm modification is dependent on host genotype in Drosophila. Proc R Soc Lond Ser B, 2001, 268(1485): 2565–2570
Braig H R, Zhou W, Dobson S L, et al. Cloning and characterization of gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipentis. J Bacteriol, 1998, 180(9): 2373–2378
Peng Y, Nielsen J E, Cunningham J P, et al. Wolbachia infection alters olfactory cued locomotion in Drosophila. Appl Environ Microbi, 2008, 74(13): 3943–3948
O’Neill S L, Giordana R, Colbert A M E, et al. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci USA, 1992, 89(7): 2699–2702
Dong P, Wang J J. Reproductive manipulation of Wolbachia to its hosts (In Chinese). Chin Bull Entomol, 2006, 43(3): 288–294
Ruang-Areerate T, Kittayapong P. Wolbachia trans-infection in Aedes aegypti: A potential gene driver of dengue vectors. Proc Natl Acad Sci USA, 2006, 103(33): 12534–12539
Duron O, Labbé P, Berticat C, et al. High Wolbachia density correlates with cost of infection for insecticide resistant Culex pipiens mosquitoes. Evolution, 2006, 60(2): 303–314
Xi Z, Gavotte L, Xie Y, et al. Genome-wide analysis of the interaction between the endosymbiotic bacterium Wolbachia and its Drosophila host. BMC Genomics, 2008, 9(1): 1
Pfarr K M, Heider U, Schmetz C, et al. The mitochondrial heat shock protein 60 (HSP60) is up-regulated in Onchocerca volvulus after the depletion of Wolbachia. Parasitology, 2008, 135(4): 529–538
Hotopp J C, Clark M E, Oliveira D C, et al. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science, 2007, 317(5845): 1753–1756
Larsson M C, Domingos A I, Jones W D, et al. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron, 2004, 43(15): 703–714
Sato K, Pellegrino M, Nakagawa T, et al. Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature, 2008, 452(7190): 1002–1006
Wicher D, Schafer R, Bauernfeind R, et al. Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature, 2008, 452(7190): 1007–1011
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Supported by National Natural Science Foundation of China (Grant No. 30870284)
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Peng, Y., Wang, Y. Infection of Wolbachia may improve the olfactory response of Drosophila . Chin. Sci. Bull. 54, 1369–1375 (2009). https://doi.org/10.1007/s11434-009-0183-6
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DOI: https://doi.org/10.1007/s11434-009-0183-6