Structure and function of the bacterial community associated with the mediterranean fruit fly

Insect Symbiosis

Volumn 3, Issue , 2008, Pages 251-272

  Behar, Adi ^a   Ben Yosef, Michael ^a   Lauzon, Carol R ^b   Yuval, Boaz ^a   Jurkevich, Edouard ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 73449122732     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1201/9781420064117     Document Type: Chapter

References (106)

1. Akkermans, A. D. L. Van Elsas, J. D., and De Bruijn, F.J. (2004). Molecular microbial ecology manual, 2nd ed. Kluwer Academic Publishers, Dordrecht.
2. Apidianakis, Y., Mindrinos, M. N., Xiao, W., et al. (2005). Profiling early infection responses: Pseudomonas aeruginosa eludes host defenses by suppressing antimicrobial peptide gene expression Proc. Nat. Acad. Sci. U.S.A. 102: 2573-2578.
3. Barneah, O., Ben-Dov, E., Kramarsky-Winter, E., et al. (2007). Characterization of black band disease in Red Sea stony corals. Environ. Microbiol. 9: 1995-2006.
4. Behar, A, Jurkevitch, E, and Yuval, B (2008a) Bringing back the fruit into fruit fly-bacteria interactions. Mol. Ecol. 17: 1375-1386.
5. 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.
6. Behar, A, Yuval, B, and Jurkevitch, E (2008b) Community structure of the Mediterranean fruit fly microbiota: seasonal and spatial sources of variation. Israel J. Ecol. Evol. (in press).
7. Ben-Dov, E., Shapiro, O. H., Siboni, N., et al. (2006). Advantage of using inosine at the 3 ' termini of 16S rRNA gene universal primers for the study of microbial diversity Appl. Environ. Microbiol. 72: 6902-6906
8. Ben-Yosef, M, Jurkevitch, E, and Yuval, B (2008) Effect of bacteria on nutritional status and reproductive success of the Mediterranean fruit fly Ceratitis capitata. Physiolog. Entomol. 33: 145-154.
9. Blay, S., and Yuval, B. (1997). Nutritional correlates of reproductive success of male Mediterranean fruit flies (Diptera: Tephritidae). Animal Behav. 54: 59-66.
10. Breznak, J.A. (1982). Intestinal microbiota of termites and other xylophagous insects. Ann. Rev. Microbiol. 36: 323-343.
11. Breznak, J.A., Brill, W.J., Mertins, J.W., et al. (1973). Nitrogen-fixation in termites. Nature 244: 577-579
12. Bryant, D A, Costas, A M G, Maresca, J A, et al (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic acidobacterium. Science 317: 523-526.
13. Capuzzo, C., Firrao, G., Mazzon, L., et al. (2005). –Candidatus Erwinia dacicola,— a coevolved symbiotic bacterium of the olive fly Bactrocera oleae (Gmelin). Int. J. System. Evol. Microbiol. 55: 1641-1647
14. Cochran, D.G. (1985). Nitrogen-excretion in cockroaches. Ann. Rev. Entomol. 30: 29-49.
15. Corby-Harris, V, Pontaroli, A C, Shimkets, L J, et al (2007) Geographical distribution and diversity of bacteria associated with natural populations of Drosophila melanogaster Appl. Environ. Microbiol. 73: 3470-3479.
16. Cox, C R, and Gilmore, M S (2007) Native microbial colonization of Drosophila melanogaster and its use as a model of Enterococcus faecalis pathogenesis. Infec. Immun. 75: 1565-1576.
17. Cox-Foster, D L, Conlan, S, Holmes, E C, et al (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318: 283-287
18. Cruden, D L, and Markovetz, A J (1987) Microbial ecology of the cockroach gut Ann. Rev. Microbiol 41: 617-643
19. Daser, U., and Brandl, R. (1992). Microbial gut floras of 8 species of tephritids. Biol. J. Linn. Soc. 45: 155-165.
20. Diaz-Fleischer, F., Papaj, D. R., Prokopy, R.J., et al. (2000). Evolution of fruit fly oviposition behavior. In Fruit Flies, Phylogeny and Evolution of Behavior (M. Aluja and A. Norrbom Eds.), pp. 811-841. CRC, Boca Raton, FL
21. Dillon, R.J., and Dillon, V.M. (2004). The gut bacteria of insects: nonpathogenic interactions. Ann. Rev. Entomol. 49: 71-92.
22. Dillon, R.J., Vennard, C.T., and Charnley, A. K. (2000). Pheromones—exploitation of gut bacteria in the locust Nature 403: 851-851
23. Dillon, R.J., Vennard, C.T., and Charnley, A. K. (2002). A note: gut bacteria produce components of a locust cohesion pheromone J. Appl. Microbiol 92: 759-763
24. Dobson, S. L. (2003). Wolbachia pipientis: impotent by association. In Insect Symbiosis (K. Bourtzis and T. A. Miller, Eds.), pp. 199-216. CRC, Boca Raton, FL.
25. Donovan, S E, Purdy, K J, Kane, M D, et al (2004) Comparison of Euryarchaea strains in the guts and food-soil of the soil-feeding termite Cubitermes fungifaber across different soil types Appl. Environ. Microbiol. 70: 3884-3892.
26. Drew, R A I, and Faye, H A (1988) Elucidation of the roles of ammonia and bacteria in the attraction of Dacus tryoni (Froggatt) (Queensland fruit fly) to proteinaceous suspensions. J. Plant Protect. Trop. 5: 127-130.
27. 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.
28. Drew, R A I, and Lloyd, A C (1991) Bacteria in the life cycle of tephritid fruit flies In Microbial Mediation of Plant-Herbivore Interactions (P. Barbarosa et al., Eds.), pp. 441-465. John Wiley & Sons, New York.
29. Drew, R. A. I., and Yuval, B. (2000). The evolution of fruit fly feeding behavior. In Fruit Flies, Phylogeny and Evolution of Behavior (M. Aluja and A. Norrbom, Eds.), pp. 731-749. CRC, Boca Raton, FL.
30. Egert, M., Wagner, B., Lemke, T., et al. (2003). Microbial community structure in midgut and hindgut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae) Appl. Environ. Microbiol. 69: 6659-6668.
31. Epsky, N. D., Heath, R. R., Dueben, B. D., et al. (1998). Attraction of 3-methyl-1-butanol and ammonia identified from Enterobacter agglomerans to Anastrepha suspensa. J. Chem. Ecol. 24: 1867-1880.
32. Favia, G., Ricci, I., Damiani, C., et al. (2007). Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proc. Nat. Acad. Sci. U.S.A. 104: 9047-9051.
33. Field, S. A., Kaspi, R., and Yuval, B. (2002). Why do calling medflies (Diptera: Tephritidae) cluster? Assessing the empirical evidence for models of medfly lek evolution. Flor. Entomol. 85: 63-72.
34. Fitt, G. P., and O'Brien, 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.
35. Fujii, J.K., and Tamashiro, M. (1972). Nosema tephritidae sp. N., a microsporidium pathogen of the oriental fruit fly, Dacus dorsalis Hednel. Proc. Haw. Entomol. Soc. 21: 191-203.
36. Fukatsu, T., and Nikoh, N. (2000). Endosymbiotic microbiota of the bamboo pseudococcid Antonina crawii (Insecta, Homoptera) Appl. Environ. Microbiol 66: 643-650
37. Galun, R, Gothilf, S, Blondheim, S, et al (1985) Comparison of aggregation and feeding responses by normal and irradiated fruit flies Ceratitis capitata and Anastrepha suspensa (Diptera: Tephritidae). Environ. Entomol. 14: 726-732.
38. Green, S.J., and Minz, D. (2005). Suicide polymerase endonuclease restriction, a novel technique for enhancing PCR amplification of minor DNA templates. Appl. Environ. Microbiol. 71: 4721-4727
39. Grimont, P A D, and Grimont, F (1978) Biotyping of Serratia marcescens and its use in epidemiological studies J. Clin. Microbiol 8: 73-83
40. Hagen, K S (1966) Dependence of Olive fly, Dacus Oleae, larvae on symbiosis with Pseudomonas savastanoi for utilization of olive Nature 209: 423
41. Hilbi, H, Weber, S S, Ragaz, C, et al (2007) Environmental predators as models for bacterial pathogenesis Environ. Microbiol 9: 563-575
42. Hosokawa, T, Kikuchi, Y, Nikoh, N, et al (2006) Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLOS Biol. 4: 1841-1851.
43. Howard, D.J., Bush, G. L., and Breznak, J. A. (1985). The evolutionary significance of bacteria associated with Rhagoletis. Evolution. 39: 405-417
44. Huber, J A, Mark Welch, D, Morrison, H G, et al (2007) Microbial population structures in the deep marine biosphere. Science 318: 97-100.
45. Ikeda-Ohtsubo, W., Desai, M., Stinglt, U., et al. (2007). Phylogenetic diversity of –Endomicrobia— and their specific affiliation with termite gut flagellates. Microbiol.-Sgm. 153: 3458-3465.
46. Judd, G.J.R., and Borden, J.H. (1992). Aggregated oviposition in Delia antiqua (Meigen)—a case for mediation by semiochemicals. J. Chem. Ecol. 18: 621-635.
47. Kaspi, R., Mossinson, S., Drezner, T., et al. (2002). Effects of larval diet on development rates and reproductive maturation of male and female Mediterranean fruit flies Physiol. Entomol 27: 29-38
48. Kikuchi, Y., Hosokawa, T., and Fukatsu, T. (2007). Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl. Environ. Microbiol. 73: 4308-4316.
49. Kikuchi, Y., Meng, X.Y., and Fukatsu, T. (2005). Gut symbiotic bacteria of the genus Burkholderia in the broad-headed bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera: Alydidae) Appl. Environ. Microbiol 71: 4035-4043
50. Kittayapong, P., Milne, J.R., Tigvattananont, S., et al. (2000). Distribution of the reproduction-modifying bacteria, Wolbachia, in natural populations of tephritid flies in Thailand Sci. Asia 26: 93-103
51. Kneip, C., Lockhart, P., Voss, C., et al. (2007). Nitrogen fixation in eukaryotes—new models for symbiosis. BMC Evol. Biol. 7.
52. Kuzina, L V, Peloquin, J J, Vacek, D C, et al (2001) Isolation and identification of bacteria associated with adult laboratory Mexican fruit flies, Anastrepha ludens (Diptera: Tephritidae) Curr. Microbiol 42: 290-294
53. Lacava, P.T., Parker, J., Andreote, F. D., et al. (2007). Analysis of the bacterial community in glassywinged sharpshooter heads. Entomol. Res. 37: 261-266.
54. Lam, K, Babor, D, Duthie, B, et al (2007) Proliferating bacterial symbionts on house fly eggs affect oviposition behaviour of adult flies. Animal Beh. 74: 81-92.
55. Lauzon, C R (2003) Symbiotic relationships of tephritids In Insect Symbiosis (K Bourtzis and T A Miller, Eds.), pp. 115-129. CRC, Boca Raton, FL.
56. Lauzon, C R, Bussert, T G, Sjogren, R E, et al (2003) Serratia marcescens as a bacterial pathogen of Rhagoletis pomonella flies (Diptera: Tephritidae). Eur. J. Entomol. 100: 87-92.
57. Lauzon, C R, and Potter, S E (2008) Visual description of radiation-induced tissue and cellular damage in the midgut of Ceratitis capitata Wiedemann (Diptera: Tephritidae) and Anastrepha ludens (Diptera: Tephritidae) used for sterile insect technique Ann. Entomol. Soc. Am. (in press)
58. Lauzon, C R, McCombs, S D, and Potter, S E (2008) Vertical passage of Enterobacter agglomerans and Klebsiella pneumoniae in Ceratitis capitata Weidemann, the Mediterranean fruit fly Ann. Entomol. Soc. Am. (in press)
59. 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
60. Lauzon, C R, Sjogren, R E, Wright, S E, et al (1998) Attraction of Rhagoletis pomonella (Diptera: Tephritidae) flies to odor of bacteria: apparent confinement to specialized members of Enterobacteriaceae Environ. Entomol 27: 853-857
61. MacCollom, G.B., Lauzon, C.R., Payne, E. B., et al. (1994). Apple maggot (Diptera: Tephritidae) trap enhancement with washed bacterial cells. Environ. Entomol. 23: 354-359.
62. MacCollom, G. B., Lauzon, C. R., Weires, R.W., et al. (1992). Attraction of adult apple maggot (Diptera, Tephritidae) to microbial isolates J. Econ. Entomol 85: 83-87
63. Manousis, T., and Moore, N. F. (1987). Cricket paralysis virus, a potential control agent for olive fruit fly, Dacus oleae Gmel Appl. Environ. Microbiol 53: 142-148
64. Marchini, D., Rosetto, M., Dallai, R., et al. (2002). Bacteria associated with the oesophageal bulb of the medfly Ceratitis capitata (Diptera: Tephritidae). Curr. Microbiol. 44: 120-124.
65. Margulies, M., Egholm, M., Altman, W. E., et al. (2005). Genome sequencing in microfabricated highdensity picolitre reactors Nature 437: 376-380
66. Martinez, A.J., Robacker, D.C., Garcia, J.A., et al. (1994). Laboratory and field olfactory attraction of the Mexican fruit-fly (Diptera: Tephritidae) to metabolites of bacterial species. Flor. Entomol. 77: 117-126.
67. 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(6): 1277-1287.
68. Metzker, M.L. (2005). Emerging technologies in DNA sequencing. Gen. Res. 15: 1767-1776.
69. Mohr, K I, and Tebbe, C C (2006) Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field. Environ. Microbiol. 8: 258-272.
70. Murphy, K. M., Macrae, I.C., and Teakle, D. S. (1988). Nitrogenase activity in the Queensland fruit fly, Dacus tryoni. Aus. J. Biol. Sci. 41: 447-451.
71. Murphy, K M, Teakle, D S, and Macrae, I C (1994) Kinetics of colonization of adult Queensland fruit-flies (Bactrocera tryoni) by dinitrogen-fixing alimentary-tract bacteria Appl. Environ. Microbiol. 60: 2508-2517.
72. Nardi, J B, Mackie, R I, and Dawson, J O (2002) Could microbial symbionts of arthropod guts contribute significantly to nitrogen fixation in terrestrial ecosystems? J. Insect Physiol. 48: 751-763.
73. Niyazi, N, Lauzon, C R, and Shelly, T E (2004) Effect of probiotic adult diets on fitness components of sterile male Mediterranean fruit flies (Diptera: Tephritidae) under laboratory and field cage conditions. J. Econ. Entomol. 97: 1570-1580.
74. Page, F., Altabe, S., Hugouvieux-Cotte-Pattat, N., et al. (2001). Osmoregulated periplasmic glucan synthesis is required for Erwinia chrysanthemi pathogenicity J. Bacteriol 183: 3134-3141
75. Papadopoulos, N T, Katsoyannos, B I, Kouloussis, N A, et al (1998) Effect of adult age, food, and time of day on sexual calling incidence of wild and mass-reared Ceratitis capitata males. Entomol. Exp. Appl. 89: 175-182.
76. Petri, L (1909) Ricerche sopra i batteri intestinali della mosca olearia Memorie della Regia Stazione di Patologia Vegetale di Roma, Roma
77. Plus, N., Veyrunes, J.C., and Cavalloro, R. (1981a). Endogenous viruses of Ceratitis capitata Wied. Jrc Ispra strain, and of Ceratitis capitata permanent cell-lines. Ann. Virol. 132: 91-100.
78. Plus, N, Gissman, L, Veyrunes, J C, et al (1981b) Reoviruses of Drosophila and Ceratitis populations and of Drosophila cell-lines—a possible new genus of the Reoviridae family Ann. Virol 132: 261-265
79. Podolsky, R D (1994) Temperature and water viscosity—physiological versus mechanical effects on suspension-feeding. Science 265: 100-103.
80. Potrikus, C.J., and Breznak, J.A. (1980a). Uric-acid degrading bacteria in guts of termites [Reticulitermes flavipes (Kollar)]. Appl. Environ. Microbiol. 40: 117-124.
81. Potrikus, C J, and Breznak, J A (1980b) Anaerobic degradation of uric-acid by gut bacteria of termites. Appl. Environ. Microbiol. 40: 125-132.
82. Potrikus, C J, and Breznak, J A (1981) Gut bacteria recycle uric-acid nitrogen in termites—a strategy for nutrient conservation. Proc. Nat. Acad. Sci. U.S.A.-Biol. Sci. 78: 4601-4605.
83. Prokopy, R J, Cooley, S S, Galarza, L, et al (1993) Bird droppings compete with bait sprays for Rhagoletis pomonella (Walsh) flies (Diptera, Tephritidae) Can. Entomol 125: 413-422
84. 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.
85. Reeson, A. F., Jankovic, T., Kasper, M. L., et al. (2003). Application of 16S rDNA-DGGE to examine the microbial ecology associated with a social wasp Vespula germanica. Insect Mol. Biol. 12: 85-91.
86. Riegler, M., and Stauffer, C. (2002). Wolbachia infections and superinfections in cytoplasmically incompatible populations of the European cherry fruit fly Rhagoletis cerasi (Diptera, Tephritidae) Mol. Ecol 11: 2425-2434
87. Robacker, D.C., and Bartelt, R.J. (1997). Chemicals attractive to Mexican fruit fly from Klebsiella pneumoniae and Citrobacter freundii cultures sampled by solid-phase microextraction J. Chem. Ecol 23: 2897-2915
88. Robacker, D C, and Flath, R A (1995) Attractants from Staphylococcus aureus cultures for the Mexican fruit fly, Anastrepha ludens. J. Chem. Ecol. 28: 1549-1563.
89. Robacker, D.C., and Lauzon, C.R. (2002). Purine metabolizing capability of Enterobacter agglomerans affects volatiles production and attractiveness to Mexican fruit fly J. Chem. Ecol 28: 1549-1563
90. Robacker, D.C., Martinez, A.J., Garcia, J. A., et al. (1998). Volatiles attractive to the Mexican fruit fly (Diptera: Tephritidae) from eleven bacteria taxa. Flor. Entomol. 81: 497-508.
91. Rocha, L. S., Mascarenhas, R.O., Perondini, A.L.P., et al. (2005). Occurrence of Wolbachia in Brazilian samples of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) Neotrop. Entomol 34: 1013-1015
92. Rohlfs, M, and Hoffmeister, T S (2003) An evolutionary explanation of the aggregation model of species coexistence. Proc. R. Soc. Lond. B-Biol. Sci. 270: S33-S35.
93. Rohlfs, M, Obmann, B, and Petersen, R (2005) Competition with filamentous fungi and its implication for a gregarious lifestyle in insects living on ephemeral resources Ecol. Entomol 30: 556-563
94. Rossiter, M.C., Howard, D.J., and Bush, G. L. (1983). Symbiotic bacteria of Rhagoletis pomonella. In Fruit Flies of Economic Importance (R Cavalloro, Ed), pp 77-84 Balkema, Rotterdam
95. Selivon, D., Perondini, A.L.P., Ribeiro, A.F., et al. (2002). Wolbachia endosymbiont in a species of the Anastrepha fraterculus complex (Diptera: Tephritidae). Invert. Reprod. Dev. 42: 121-127.
96. Silva, F., Alcazar, A., Macedo, L. L. P., et al. (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
97. Steinhaus, E A (1959) Serratia marcescens Bizio as an insect pathogen Hildgardia 28: 351
98. Tsitsipis, J. A. (1989). Nutrition: requirements. In Fruit Flies, Their Biology, Natural Enemies and Control (A. S. Robinson and G. Hooper, Eds.), pp. 103-119. Elsevier, Amsterdam.
99. Van Elsas, J., Jansson, J. K., and Trevors, J.T. (2007). Modern Soil Microbiology. CRC Press, Boca Raton, FL. Von Dohlen, C D, Kohler, S, Alsop, S T, et al (2001) Mealybug beta-proteobacterial endosymbionts contain gamma-proteobacterial symbionts Nature 412: 433-436.
100. Wang, Y.J., Stingl, U., Anton-Erxleben, F., et al. (2004). “Candidatus Hepatincola porcellionum” gen. nov, sp nov, a new, stalk-forming lineage of Rickettsiales colonizing the midgut glands of a terrestrial isopod Arch. Microbiol 181: 299-304
101. Warnecke, F., Luginbuhl, P., Ivanova, N., et al. (2007). Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite Nature 450: 560-565
102. Yuval, B, and Hendrichs, J (2000) Behavior of flies in the genus Ceratitis (Dacinae: Ceratidini) In Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior (M. Aluja and A. Norrbom, Eds.), pp. 429-456 CRC Press.
103. Boca Raton, FL Yuval, B, Kaspi, R, Shloush, S, et al (1998) Nutritional reserves regulate male participation in Mediterranean fruit fly leks. Ecol. Entomol. 23: 211-215.
104. Zabalou, S, Riegler, M, Theodorakopoulou, M, et al (2004) Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control Proc. Nat. Acad. Sci. U.S.A 101: 15042-15045
105. Zhang, Y.P., Pohlmann, E.L., Ludden, P.W., et al. (2001). Functional characterization of three GlnB homologs in the photosynthetic bacterium Rhodospirillum rubrum: roles in sensing ammonium and energy status J. Bacteriol. 183: 6159-6168
106. Zinder, D. E., and Dworkin, M. (2000). Morphological and physiological diversity. In The Prokaryotes (M Dworkin et al, Eds) Springer Verlag, New York