Riding the Trojan horse: Combating pest insects with their own symbionts

Microbial Biotechnology

Volumn 4, Issue 5, 2011, Pages 620-627

  Jurkevitch, Edouard ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

DNA 16S; NITROGEN DERIVATIVE;

COMMUNITY STRUCTURE; DIET; DNA REPAIR; FITNESS; FOOD INTAKE; HORSEBACK RIDING; HOST; INOCULATION; INSECT; INTESTINE; KLEBSIELLA; LARVA; MATING; MEDITERRANEAN FRUIT FLY; MICROFLORA; NONHUMAN; NUTRITION; SHORT SURVEY; SURVIVAL; SYMBIONT; TEPHRITIDAE; WOLBACHIA;

ANIMALS; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; FEMALE; MALE; SYMBIOSIS; TEPHRITIDAE;

ANIMALIA; BACTROCERA OLEAE; CERATITIS CAPITATA; EQUIDAE; HEXAPODA; KLEBSIELLA; TEPHRITIDAE;

EID: 84860408273     PISSN: 17517907     EISSN: 17517915     Source Type: Journal    
DOI: 10.1111/j.1751-7915.2011.00249.x     Document Type: Short Survey

References (73)

1. Amiot, M.-J., Fleuriet, A., and Macheix, J.-J. (1989) Accumulation of oleuropein derivatives during olive maturation. Phytochemistry 28: 67-69.
2. Baumann, P., Moran, N.A., and Baumann, L. (2006) Bacteriocyte-associated endosymbionts of insects. In The Prokaryotes. Volume 1: Symbiotic associations, Biotechnology, Applied Microbiology. Dworkin, M., Rosenberg, E., Schleifer, K.-H., and Stackebrandt, E. (eds). New York, USA: Springer, pp. 403-438.
3. Beard, C.B., O'Neill, S.L., Mason, P., Mandelco, L., Woese, C.R., Tesh, R.B., etal. (1992) Genetic transformation and phylogeny of bacterial symbionts from tsetse. Insect Mol Biol 1: 123-131.
4. Behar, A., Yuval, B., and Jurkevitch, E. (2005) Enterobacteria-mediated nitrogen fixation in natural populations of the fruit fly, Ceratitis capitata. Mol Ecol 14: 2637-2643.
5. Behar, A., Jurkevitch, E., and Yuval, B. (2008a) Bringing back the fruit into fruit fly-bacteria interactions. Mol Ecol 17: 1375-1386.
6. Behar, A., Yuval, B., and Jurkevitch, E. (2008b) Gut bacterial communities in the Mediterranean fruit fly (Ceratitis capitata) and their impact on host longevity. J Insect Physiol 54: 1377-1383.
7. Behar, A., Ben-Yosef, M., Lauzon, C.R., Yuval, B., and Jurkevitch, E. (2008c) Structure and function of the bacterial community associated with the Mediterranean fruit fly. In Insect Symbiosis. Bourtzis, K., and Miller, T. (eds). Boca Raton, USA: CRC, pp. 251-271.
8. Ben Ami, E., Yuval, B., and Jurkevitch, E. (2010) Manipulation of the microbiota of mass-reared Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae) improves sterile male sexual performance. ISME J 4: 28-37.
9. Ben-Yosef, M., Jurkevitch, E., and Yuval, B. (2008a) Effect of bacteria on nutritional status and reproductive success of the Mediterranean fruit fly Ceratitis capitata. Physiol Entomol 33: 145-154.
10. Ben-Yosef, M., Behar, A., Jurkevitch, E., and Yuval, B. (2008b) Bacteria-diet interactions affect longevity in the medfly -Ceratitis capitata. J Appl Entomol 132: 690-694.
11. Ben-Yosef, M., Aharon, Y., Jurkevitch, E., and Yuval, B. (2010) Give us the tools and we will do the job: symbiotic bacteria affect olive fly fitness in a diet dependent fashion. Proc R Soc Lond B Biol Sci 277: 1545-1552.
12. Brownlie, J.C., Cass, B.N., Riegler, M., Witsenburg, J.J., Iturbe-Ormaetxe, I., McGraw, E.A., and O'Neill, S.L. (2009) Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Pathog 5: e1000368.
13. Capuzzo, C., Firrao, G., Mazzon, L., Squartini, A., and Girolami, V. (2005) 'Candidatus Erwinia dacicola', a coevolved symbiotic bacterium of the olive fly Bactrocera oleae (Gmelin). Int J Syst Evol Microbiol 55: 1641-1647.
14. Chaston, J., and Goodrich-Blair, H. (2010) Common trends in mutualism revealed by model associations between invertebrates and bacteria. FEMS Microbiol Rev 34: 41-58.
15. Christenson, L.D., and Foote, R.H. (1960) Biology of fruit flies. Annu Rev Entomol 5: 171-192.
16. Conord, C., Despres, L., Vallier, A., Balmand, S., Miquel, C., etal. (2008) Long-term evolutionary stability of bacterial endosymbiosis in Curculionoidea: additional evidence of symbiont replacement in the Dryophthoridae family. Mol Biol Evol 25: 859-868.
17. Daser, U., and Brandl, R. (1992) Microbial gut floras of 8 species of Tephritids. Biol J Linn Soc 45: 155-165.
18. Dean, M.D. (2006) A Wolbachia-associated fitness benefit depends on genetic background in Drosophila simulans. Proc R Soc B 273: 1415-1420.
19. Douglas, A. (2009) The microbial dimension in insect nutritional ecology. Funct Ecol 23: 38-47.
20. Drew, R.A.I., and Lloyd, A.C. (1987) Relationship of fruit-flies (Diptera, Tephritidae) and their bacteria to host plants. Ann Entomol Soc Am 80: 629-636.
21. Drew, R.A.I., and Yuval, B. (2000) The evolution of fruit fly feeding behavior. In Fruit Flies, Phylogeny and Evolution of Behavior. Aluja, M., and Norrbom, A. (eds). Boca Raton, USA: CRC, pp. 731-749.
22. Estes, A.M., Hearn, D.J., Bronstein, J.L., and Pierson, E.A. (2009) The olive fly endosymbiont, 'Candidatus Erwinia dacicola', switches from an intracellular existence to an extracellular existence during host insect development. Appl Environ Microbiol 75: 7097-7106.
23. Euzeby, J. (2010) List of prokaryotic names with standing in nomenclature [WWW document]. URL.
24. Evenhuis, N.L., Pape, T., Pont, A.C., and Thompson, F.C. (2008) The Diptera Site [WWW document]. URL.
25. Feldhaar, H., Straka, J., Krischke, M., Berthold, K., Stoll, S., Mueller, M.J., and Gross, R. (2007) Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia. BMC Biol 5: 48.
26. Fitt, G.P., and Obrien, R.W. (1985) Bacteria associated with 4 species of Dacus (Diptera, Tephritidae) and their role in the nutrition of the larvae. Oecologia 67: 447-454.
27. Gavriel, S., Jurkevitch, E., Gazit Y., and Yuval, B. (2011) Bacterially enriched diet improves sexual performance of sterile male Mediterranean fruit flies. J Appl Entomol (in press).
28. Gevers, D., Cohan, F.M., Lawrence, J.G., Spratt, B.G., Coenye, T., Feil, E.J., etal. (2005) Re-evaluating prokaryotic species. Nat Rev Microbiol 3: 733-739.
29. Hagen, K.S. (1966) Dependence of the olive fly, Dacus oleae, larvae on symbiosis with Pseudomonas savastanoi for the utilization of olive. Nature 209: 423-424.
30. Hagen, K.S., and Tassan, R.L. (1972) Exploring nutritional roles of extracellular symbiotes on the reproduction of honeydews feeding adult Chrysopids and Tephritids. In Insect and Mite Nutrition. Rodriguez, J.G. (ed.) Amsterdam: North-Holland, pp. 323-351.
31. Headrick, D.H., and Goeden, R.D. (1994) Reproductive behavior of California fruit flies and the classification and evolution of Tephritidae (Diptera) mating systems. Stud Dipterol 1: 195-252.
32. Hendrichs, J., Franz, G., and Rendon, P. (1995) Increased effectiveness and applicability of the sterile insect technique through male-only releases for control of Mediterranean fruit flies during fruiting seasons. J Appl Entomol 119: 371-377.
33. Howard, D.J., Bush, G.L., and Breznak, J.A. (1985) The evolutionary significance of bacteria associated with Rhagoletis. Evolution 39: 405-417.
34. Kato, T. (1981) Major nitrogen compounds transported in xylem vessels from roots to top in Citrus trees. Physiol Plant 52: 275-279.
35. Kaspi, R., Mossinson, S., Drezner, T., Kamensky, B., and Yuval, B. (2002) Effects of larval diet on development rates and reproductive maturation of male and female Mediterranean fruit flies. Physiol Entomol 27: 29-38.
36. Klassen, W., and Curtis, C.F. (2005) History of the sterile insect technique. In Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Dyck, V.A., Hendrichs, J., and Robinson, A.S. (eds). Dordrecht, the Netherlands: Springer, pp. 3-38.
37. Koukou, K., Pavlikaki, H., Kilias, G., Werren, J.H., Bourtzis, K., and Alahiotis, S.N. (2006) Influence of antibiotic treatment and Wolbachia curing on sexual isolation among Drosophila melanogaster cage populations. Evolution 60: 87-96.
38. Kounatidis, I., Crotti, E., Sapountzis, P., Sacchi, L., Rizzi, A., Chouaia, B., etal. (2009) Acetobacter tropicalis is a major symbiont of the olive fruit fly (Bactrocera oleae). Appl Environ Microbiol 75: 3281-3288.
39. Kuzina, L.V., Peloquin, J.J., Vacek, D.C, and Miller, T.A. (2001) Isolation and identification of bacteria associated with adult laboratory Mexican fruit flies, Anastrepha ludens (Diptera: Tephritidae). Cur Microbiol 42: 290-294.
40. Lauzon, C.R. (2003) Symbiotic relationships of Tephritids. In Insect Symbiosis. Bourtzis, K., and Miller, T.A. (eds). Boca Raton, FL, USA: CRC, pp. 115-129.
41. Lauzon, C.R., McCombs, S.D., Potter, S.E., and Peabody, N.C. (2009) Establishment and vertical passage of Enterobacter (Pantoea) agglomerans and Klebsiella pneumoniae through all life stages of the Mediterranean fruit fly (Diptera: Tephritidae). Ann Entomol Soc Am 102: 85-95.
42. Lauzon, C.R., Sjogren, R.E., Wright, S.E., and Prokopy, R.J. (1998) Attraction of Rhagoletis pomonella (Diptera Tephritidae) flies to odor of bacteria: Apparent confinement to specialized members of Enterobacteriaceae. Environ Entomol 27: 853-857.
43. Lauzon, C.R., Sjogren, R.E., and Prokopy, R.J. (2000) Enzymatic capabilities of bacteria associated with apple maggot flies: a postulated role in attraction. J Chem Ecol 26: 953-967.
44. Lefevre, C., Charles, H., Vallier, A., Delobel, B., Farrell, B., and Heddi, A. (2004) Endosymbiont phylogenesis in the Dryophthoridae weevils: evidence for bacterial replacement. Mol Biol Evol 21: 965-973.
45. Liquido, N., Shinoda, L.A., and Cunningham, R.T. (1991) Host plants of the Mediterranean fruit fly (Diptera: Tephritidae): an annotated world review. Miscellaneous Publications of the Entomological Society of America, Number 77.
46. Marchini, D., Rosetto, M., Dallai, R., and Marry, L. (2002) Bacteria associated with the oesophageal bulb of the medfly Ceratitis capitata (Diptera Tephritidae). Curr Microbiol 44: 120-124.
47. Martinez, A.J., Robacker, D.C., Garcia, J.A., and Esau, K.L. (1994) Laboratory and field olfactory attraction of the Mexican fruit-fly (Diptera: Tephritidae) to metabolites of bacterial species. Flo Entomol 77: 117-126.
48. Mayhew, P.J. (2007) Why are there so many insect species? Biol Rev 82: 425-454.
49. Mazzon, L., Piscedda, A., Simonato, M., Martinez-Sanudo, I., Squartini, A., and Girolami, V. (2008) Presence of specific symbiotic bacteria in flies of the subfamily Tephritinae (Diptera Tephritidae) and their phylogenetic relationships: proposal of 'Candidatus Stammerula tephritidis'. Int J Syst Evol Microbiol 58: 1277-1287.
50. McCutcheon, J., and Moran, N.A. (2007) Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc Natl Acad Sci USA 104: 19392-19397.
51. Moran, N.A. (1996) Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci USA 93: 2873-2878.
52. O'Neill, S.L., and Karr, T.L. (1990) Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature 348: 178-180.
53. Pais, R., Lohs, C., Wu, Y., Wang, J., and Aksoy, S. (2008) The obligate mutualist Wigglesworthia glossinidia influences reproduction, digestion, and immunity processes of its host, the Tsetse fly. Appl Environ Microbiol 74: 5965-5974.
54. Petri, L. (1909) Ricerche Sopra i Batteri Intestinali della Mosca Olearia. Roma: Memorie della Regia Stazione di Patologia Vegetale di Roma.
55. Raghu, S., Clarke, A.R., and Bradley, J. (2002) Microbial mediation of fruit fly-host plant interactions: Is the host plant the "centre of activity"? Oikos 97: 319-328.
56. Rosenberg, E., Sharon, G., and Zilber-Rosenberg, I. (2009) The hologenome theory of evolution contains Lamarckian aspects within a Darwinian framework. Environ Microbiol 11: 2959-2962.
57. Rossiter, M.C., Howard, D.J., and Bush, G.L. (1983) Symbiotic bacteria of Rhagoletis pomonella. In Fruit flies of economic importance. Cavalloro, R. (ed.). Balkema: CRC Press, pp.77-84.
58. Ryan, D., Robards, K., and Lavee, S. (1999) Accumulation of oleuropein derivatives during olive maturation. Int J Food Sci Technol 34: 265-274.
59. Ryu, J.-H., Kim, S.-H., Lee, H.-Y., Bai, J.Y., Nam, Y.-D., Bae, J.-W., etal. (2008) Innate immune homeostasis by the homeobox gene Caudal and commensal-gut mutualism in Drosophila. Science 319: 777-782.
60. Sandström, J., and Pettersson, J. (1994) Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance. J Insect Physiol 40: 947-955.
61. Silva, F., Alcazar, A., Macedo, L.L.P., Oliveira, A.S., Macedo, F.P., Abreu, L.R., etal. (2006) Digestive enzymes during development of Ceratitis capitata (Diptera:Tephritidae) and effects of SBTI on its digestive serine proteinase targets. Insect Biochem Mol Biol 36: 561-569.
62. Stammer, H.J. (1929) Die bakteriensymbiose der trypetiden (Diptera). Zoomorphology 15: 481-523.
63. Tamas, I.K.L., Canback, B., Naslund, K.A., Eriksson, A.-S., Wernegreen, J.J., Sandstrom, J.P., etal. (2002) 50 Million years of genomic stasis in endosymbiotic bacteria. Science 296: 2376-2379.
64. Toh, H., Weiss, B.L., Perkin, S.A.H., Yamashita, A., Oshima, K., Hattori, M., and Aksoy, S. (2006) Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Gen Res 16: 149-156.
65. Torsvik, V., Øvreås, L., and Thingstad, T.F. (2002) Prokaryotic diversity - magnitude, dynamics, and controlling factors. Science 296: 1064-1066.
66. Tsitsipis, J.A. (1989) Nutrition: requirements. In Fruit Flies, Their Biology, Natural Enemies and Control, Vol. 3A. Robinson, A.S., and Hooper, G. (eds). Amsterdam, the Netherlands: Elsevier, pp. 103-119.
67. Turelli, M., and Hoffmann, A.A. (1991) Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353: 440-442.
68. Wackers, F.L. (2005) Suitability of (extra-) floral nectar, pollen, and honeydew as insect food sources. In Plant-Provided Food for Carnivorous Insects: Protective Mutualism and Its Applications. Wackers, F.L., van Rijn, P.C.J., and Bruin, J. (eds). Cambridge, UK: Cambridge University Press, pp. 17-74.
69. White, I.M., and Elson-Harris, M.M. (1992) Fruit Flies of Economic Significance: Their Identification and Bionomics. Wallingford, USA: CAB International.
70. Wilson, E.O. (2003) The encyclopedia of life. Trends Ecol Evol 18: 77-80.
71. Yeates, D.K., and Wiegmann, B.M. (2005) Phylogeny and evolution of Diptera: recent insight and new perspective. In The Evolutionary Biology of Flies. Yeates, D.K., and Wiegmann, B.M. (eds). New York, USA: Colombia University Press, pp. 14-44.
72. Zinder, D.E., and Dworkin, M. (2000) Morphological and physiological diversity. In The Prokaryotes. Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H., and Stackebrandt, E. (eds). New York, USA: Springer Verlag, pp. 185-220.
73. Zilber-Rosenberg, E., and Rosenberg, E. (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32: 723-735.