Give us the tools and we will do the job: Symbiotic bacteria affect olive fly fitness in a diet-dependent fashion

Proceedings of the Royal Society B: Biological Sciences

Volumn 277, Issue 1687, 2010, Pages 1545-1552

  Ben Yosef, Michael ^a   Aharon, Yael ^a   Jurkevitch, Edouard ^a   Yuval, Boaz ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Bacterial symbionts; Nutritional ecology; Tephritidae

Indexed keywords

AMINO ACID; BACTERIUM; DIET; FECUNDITY; FITNESS; FLY; HYPOTHESIS TESTING; LIFE CYCLE; LIFE HISTORY TRAIT; MORPHOLOGY; SYMBIONT;

BACTERIA (MICROORGANISMS); BACTROCERA OLEAE; TEPHRITIDAE;

EID: 77952698900     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2009.2102     Document Type: Conference Paper

References (65)

1. Bandi, C., Damiani, G., Magrassi, L., Grigolo, A., Fani, R. & Sacchi, L. 1994 Flavobacteria as intracellular symbionts in cockroaches. Proc. R. Soc. Lond B 257, 43-48. (doi:10.1098/rspb.1994.0092)
2. Baumann, P., Moran, N. & Baumann, L. 2006 Bacteriocyteassociated endosymbionts of insects. In The prokaryotes, vol. 1 (eds M. Dworkin, S. Falkow, E. Rosenberg, K. H. Schleifer & E. Stackebrandt), pp. 403-438. New York, NY: Springer Verlag.
3. Behar, A., Yuval, B. & Jurkevitch, E. 2005 Enterobacteriamediated nitrogen fixation in natural populations of the fruit fly Ceratitis capitata. Mol. Ecol. 14, 2637-2643. (doi:10.1111/j.1365-294X.2005.02615.x) (Pubitemid 41576949)
4. Behar, A., Ben-Yosef, M., Lauzon, C. R., yuval, B. & Jurkevitch, E. 2009 Structure and function of the bacterial community associated with the Mediterranean fruit fly. In Insect symbiosis (eds K Bourtzis & T. A. Miller), vol. 3, pp. 251-272. Boca Raton, FL: CRC Press.
5. Ben-Yosef, M., Jurkevitch, E. & Yuval, B. 2008a Effect of bacteria on nutritional status and reproductive success of the Mediterranean fruit fly Ceratitis capitata. Physiol. Entomol. 33, 145-154. (doi:10.1111/j.1365-3032. 2008.00617.x) (Pubitemid 351623757)
6. Ben-Yosef, M., Behar, A., Jurkevitch, E. & Yuval, B. 2008b Bacteria-diet interactions affect longevity in the medfly- Ceratitis capitata. J. Appl. Entomol. 132, 690-694. (doi:10.1111/j.1439-0418.2008.01330.x)
7. Billen, J. & Buschinger, A. 2000 Morphology and ultrastructure of a specialized bacterial pouch in the digestive tract of Tetraponera ants (Formicidae, Pseudomyrmecinae). Arthropod Struct. Dev. 29, 259-266. (doi:10.1016/ S1467-8039(00)00029-3) (Pubitemid 32524614)
8. Bourtzis, K. & Miller, T. A. (eds) 2003 Insect symbiosis. Contemporary topics in entomology, vol. 1. Boca Raton, FL: CRC Press.
9. Bourtzis, K. & Miller, T. A. (eds) 2009 Insect symbiosis. Contemporary topics in entomology, vol. 3. Boca Raton, FL: CRC Press.
10. Boush, G. M., Baerwald, R. J. & Miyazaki, S. 1969 Development of a chemically defined diet for adults of apple maggot based on amino acid analysis of honeydew. Ann. Entomol. Soc. Am. 62, 19-21.
11. Buchner, P. 1965 Endosymbiosis of animals with plant microorganisms. New York, NY: John Wiley and Sons.
12. Capuzzo, C., Firrao, G., Mazzon, L., Squartini, A. & 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. (doi:10.1099/ijs.0.63653-0)
13. Chang, C. L., Albrecht, C., El-Shall, S. S. A. & Kurashima, R. 2001 Adult reproductive capacity of Ceratitis capitata (Diptera: Tephritidae) on a chemically defined diet. Ann. Entomol. Soc. Am. 94, 702-706. (doi:10.1603/ 0013 8746(2001)094[0702:ARCOCC]2.0.CO;2)
14. Christenson, L. D. & Foote, R. H. 1960 Biology of fruit flies. Ann. Rev. Entomol. 5, 171-192. (doi:10.1146/annurev.en.05.010160.001131)
15. Cook, S. C. & Davidson, D. W. 2006 Nutritional and functional biology of exudate-feeding ants. Entomol. Exp. Appl. 118, 1-10. (doi:10.1111/j.1570- 7458.2006.00374.x)
16. Dadd, R. H. 1985 Nutrition: organisms. In Comprehensive insect physiology, biochemistry and pharmacology, vol. 4 (eds G. A. Kerkurt & L. I. Gilbert), pp. 313-390. Oxford, UK: Pergamon Press.
17. Dasch, G. A., Weiss, E. & Chang, K. P. 1984 Endosymbionts of insects. In Bergey's manual of systematic bacteriology, vol. 1 (eds N. R. Krieg & J. G. Holt), pp. 811-833. Baltimore, MD: The Williams & Wilkins Co.
18. Davidson, D. W., Cook, S. C., Snelling, R. R. & Chua, T. H. 2003 Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300, 969-972. (doi:10.1126/science.1082074)
19. Dillon, R. J. & Dillon, V. M. 2004 The gut bacteria of insects: nonpathogenic interactions. Ann. Rev. Entomol. 49, 71-92. (doi:10.1146/annurev. ento.49.061802.123416)
20. Douglas, A. E. 1998 Nutritional interactions in insectmicrobial symbioses: aphids and their symbiotic bacteria Bucknera. Ann. Rev. Entomol. 43, 17-37. (doi:10.1146/annurev.ento.43.1.17)
21. Douglas, A. E. 2006 Phloem-sap feeding by animals: problems and solutions. J. Exp. Bot. 57, 747-754. (doi:10.1093/jxb/erj067)
22. Douglas, A. E. 2009 The microbial dimension in insect nutritional ecology. Funct. Ecol. 23, 38-47. (doi:10.1111/J.1365-2435.2008.01442.x)
23. Downes, W. L. & Dahlem, G. A. 1987 Keys to the evolution of Diptera-role of Homoptera. Environ. Entomol. 16, 847-854.
24. Drew, R. A. I. & Lloyd, A. C. 1991 Bacteria in the life cycle of Tephritid fruit flies. In Microbial mediation of plantherbivore interactions (eds P. Barbarosa, V. A. Krischik & C. G. Jones), pp. 441-465. New York, NY: John Wiley & Sons.
25. Drew, R. A. I. & Yuval, B. 2000 The evolution of fruit fly feeding behaviour. In Fruit flies: phylogeny and evolution of behavior (eds M. Aluja & A. L. Norrbom), pp. 731-749. Boca Raton, FL: CRC Press.
26. Drew, R. A. L., Courtice, A. C. & Teakle, D. S. 1983 Bacteria as a natural source of food for adult fruit-flies (Diptera, Tephritidae). Oecologia 60, 279-284. (doi:10.1007/BF00376839)
27. Economopoulos, A. P., Voyadjoglou, A. V. & Giannakakis, A. 1976 Reproductive behavior and physiology of Dacus Oleae (Diptera-Tephritidae)- fecundity as affected by mating, adult diet and artificial rearing. Ann. Entomol. Soc. Am. 69, 725-729.
28. Estes, A. M. 2009 Life in a fly: The ecology and evolution of the olive fly endosymbiont. In Candidatus Erwinia dacicola. PhD thesis, University of Arizona.
29. Estes, A. M., Hearn, D. J., Bronstein, J. L. & Pierson, E. A. 2009 The olive fly endosymbiont, 'Candidatus Erwinia dacicola,' switches from an intracellular existence to an extracellular existence during host insect development. App. Environ. Microbiol. 75, 7097-7106. (doi:10.1128/AEM.00778-09)
30. Feldhaar, H., Straka, J., Krischke, M., Berthold, K., Stoll, S., Mueller, M. J. & Gross, R. 2007 Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia. BMC Biol. 5. (doi:10.1186/1741-7007-5-48)
31. Garrity, G. M. 2001 Bergey's manual of systematic bacteriology. New York, NY: Springer.
32. Girolami, V. 1973 Reperti morfo-istologici sulle batteriosimbiosi del Dacus oleae Gmelin e di altri ditteri tripetidi, in natura e negli allevamenti su substrati artificiali. Redia 54, 269-294.
33. Glockner, F. O., Zaichikov, E., Belkova, N., Denissova, L., Pernthaler, J., Pernthaler, A. & Amann, R. 2000 Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of Actinobacteria. App. Environ. Microbiol 66, 5053-5065. (doi:10.1128/AEM.66.11.5053-5065.2000)
34. Hagen, K. S. & Tassan, R. L. 1972 Exploring nutritional roles of extracellular symbiotes on the reproduction of honeydew feeding adult Chrysopids and Tephritids. In Insect and mite nutrition (ed. J. G. Rodriguez), pp. 323-351. Amsterdam, The Netherlands: North-Holland.
35. Hagen, K. S., Santas, L. & Tsecouras, A. 1963 A technique of culturing the olive fruit fly, Dacus oleae Gmel. on synthetic media under xenic conditions. In Radiation and radioisotopes applied to insects of agricultural importance, pp. 333-356. Athens, Greece: International Atomic Agency (Vienna, STI/PUB/74).
36. Ishikawa, H. 1989 Biochemical and molecular aspects of endosymbiosis in insects. Int. Rev. Cytol. 116, 1-45. (doi:10.1016/S0074-7696(08)60637-3)
37. Ishikawa, H. 2003 Insect symbiosis: an introduction. In Insect symbiosis (eds K. Bourtzis & T. A. Miller), vol. 1, pp. 1-21. Boca Raton, FL: CRC Press.
38. Kounatidis, I. et al. 2009 Acetobacter tropicalis is a major symbiont of the olive fruit fly (Bactrocera oleae). App. Environ. Microbiol. 75, 3281-3288. (doi:10.1128/AEM. 02933-3008)
39. Lauzon, C. R. 2003 Symbiotic relationships of Tephritids. In Insect symbiosis (eds K. Bourtzis & T. A. Miller), vol. 1, pp. 115-129. Boca Raton, FL: CRC Press.
40. Lemos, F. J. A. & Terra, W. R. 1991 Digestion of bacteria and the role of midgut lysozyme in some insect larvae. Comp. Biochem. Phys. B 100, 265-268. (doi:10.1016/03050491(91)90372-K)
41. Lopez-Sanchez, M. J., Neef, A., Pereto, J., Patino-Navarrete, R., Pignatelli, M., Latorre, A. & Moya, A. 2009 Evolutionary convergence and nitrogen metabolism in Blattabacterium strain Bge, primary endosymbiont of the cockroach Blattella germanica. PLoS Genet. 5, e1000721. (doi:10.1371/journal. pgen.1000721)
42. Lundgren, J. G. 2009 Relationships of natural enemies and nonprey foods. Progress in biological control. Dordrecht, The Netherlands: Springer.
43. Manousis, T & Ellar, D. J. 1988 Dacus oleae microbial symbionts. Microbiol. Sci. 5, 149-152.
44. Mazzini, M. & Vita, G. I. 1981 Identificazione submicroscopica del meccanismo di trasmissione del batterio simbionte in Dacus oleae (Diptera, Trypetidae). Redia 64, 277-301.
45. Mazzon, L., Piscedda, A., Simonato, M., Martinez-Sanudo, I., Squartin, A. & 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. (doi:10.1099/ijs.0.65287-0)
46. Miyazaki, S., Boush, G. M. & Baerwald, R. J. 1968 Amino acid synthesis by Pseudomonas melophthora, bacterial symbiote of Rhagoletis pomonella (Diptera). J. Ins. Physiol. 14, 513-518. (doi:10.1016/0022-1910(68)90066-8)
47. Petri, L. 1910 Untersuchung uber die darmbakterien der olivenffiege. Zentbl. Bakteriolog. P 26, 357-367.
48. Russell, J. A., Moreau, C. S., Goldman-Huertas, B., Fujiwara, M., Lohman, D. J. & Pierce, N. E. 2010 Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc. Natl Acad. Sci. USA 106, 21 236-21 241 (doi:10.1073/pnas.0907926106)
49. Sacchetti, P., Granchietti, A., Landini, S., Viti, C., Giovannetti, L. & Belcari, A. 2008 Relationships between the olive fly and bacteria. J. Appl. Entomol. 132, 682-689. (doi:10.1111/j.1439-0418.2008.01334.x)
50. Stammer, H. J. 1929 Die bakteriensymbiose der Trypetiden (Diptera). Zoomorphology 15, 481-523.
51. Stoll, S., Gadau, J., Gross, R. & Feldhaar, H. 2007 Bacterial microbiota associated with ants of the genus Tetraponera. Biol. J. Linnean Soc. 90, 399-412. (doi:10.1111/j.1095-8312.2006.00730.x) (Pubitemid 46302308)
52. Tamashiro, M., Westcot, D. M., Mitchell, W. C. & Jones, W. E. 1990 Axenic rearing of the oriental fruit fly Dacus dorsalis Hendel, Diptera: Tephritidae. P. Hawaii. Entomol. Soc. 30, 113-120.
53. Tsiropoulos, G. J. 1977 Reproduction and survival of adult Dacus-oleae feeding on pollens and honeydews. Environ. Entomol. 6, 390-392.
54. Tsiropoulos, G. J. 1980a Major nutritional requirements of adult Dacus oleae (Diptera, Tephritidae). Ann. Entomol. Soc. Am. 73, 251-253.
55. Tsiropoulos, G. J. 1980b The importance of vitamins in adult Dacus oleae (Diptera, Tephritidae) nutrition. Ann. Entomol. Soc. Am. 73, 705-707.
56. Tsiropoulos, G. J. 1981a Effects of varying the dietary nitrogen to carbohydrate ratio upon the biological performance of adult Dacus oleae (Diptera-Tephritidae). Arch. Int. Physiol. Biochim. Biophys. 89, 101-105. (doi:10.3109/13813458109073989)
57. Tsiropoulos, G. J. 19816 Effect of antibiotics incorporated into defined adult diets on survival and reproduction of the walnut husk fly, Rhagoletis completa Cress (Dipt, Trypetidae). J. App. Entomol. 91, 100-106.
58. Tsiropoulos, G. J. 1983 The importance of dietary aminoacids on the reproduction and longevity of adult Dacus oleae (Gmelin) (Diptera Tephritidae). Arch. Int. Physiol. Biochim. Biophys. 91, 159-164.
59. Tsiropoulos, G. J. 1984 Amino-acid synthesis in adult Dacus oleae (Gmelin) (Diptera-Tephritidae) determined with [U-C-14] glucose. Arch. Int. Physiol. Biochim. Biophys. 92, 313-316. (doi:10.3109/13813458409071172)
60. Tsitsipis, J. A. 1989 Nutrition: requirements. In Fruit flies, their biology, natural enemies and control, vol. 3A (eds A. S. Robinson & G. Hooper), pp. 103-119. Amsterdam, The Netherlands: Elsevier.
61. van Borm, S., Buschinger, A., Boomsma, J. J. & Billen, J. 2002 Tetraponera ants have gut symbionts related to nitrogen-fixing root-nodule bacteria. Proc. R. Soc. Lond. B 269, 2023-2027. (doi:10.1098/rspb.2002.2101) (Pubitemid 35177012)
62. Vijaysegaran, S., Walter, G. H. & Drew, R. A. I. 1997 Mouthpart structure, feeding mechanisms, and natural food sources of adult Bactrocera (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 90, 184-201. (Pubitemid 127639831)
63. Wackers, F. L. 2005 Suitability of (extra-)floral nectar, pollen, and honeydew as insect food sources. Plantprovided food for carnivorous insects: protective mutualism and its applications, pp. 17-74. Cambridge, UK: Cambridge University Press.
64. Zervas, G. A. 1983 Sexual and reproductive maturation in wild and lab culture olive fruit flies Dacus oleae (Gmelin) (Diptera: Tephritidae). In Fruit flies of economic importance (ed. R. Cavalloro), pp. 429-438. Rotterdam, The Netherlands: A. A. Balkema.
65. Zientz, E., Feldhaar, H., Stoll, S. & Gross, R. 2005 Insights into the microbial world associated with ants. Arch. Microbiol. 184,199-206. (doi:10.1007/s00203-005-0041-0) (Pubitemid 41627635)