Extraordinarily widespread and fantastically complex: Comparative biology of endosymbiotic bacterial and fungal mutualists of insects

Ecology Letters

Volumn 13, Issue 2, 2010, Pages 223-234

  Gibson, Cara M ^a   Hunter, Martha S ^a  

^a Environmental Research Laboratory   (United States)

Author keywords

Context dependent associations; Symbiont genomes; Symbiosis; Yeast like symbionts

Indexed keywords

BACTERIUM; ENDOSYMBIONT; EVOLUTIONARY BIOLOGY; FUNGUS; GENOME; HOST-PARASITE INTERACTION; INSECT; MUTUALISM;

ANIMAL; BACTERIUM; EVOLUTION; FUNGUS; INSECT; MICROBIOLOGY; REVIEW; SYMBIOSIS;

ANIMALS; BACTERIA; EVOLUTION; FUNGI; INSECTS; SYMBIOSIS;

ARTHROPODA; BACTERIA (MICROORGANISMS); FUNGI; HAMILTONAPHIS STYRACI YEAST-LIKE SYMBIONT; HEXAPODA;

EID: 74549117866     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/j.1461-0248.2009.01416.x     Document Type: Review

References (80)

1. Alexopoulos, C.J., Mims, C.W. Blackwell, M. (1996). Introductory Mycology. John Wiley and Sons, Inc, New York.
2. Arneodo, J.D., Bressan, A., Lherminier, J., Michel, J. Boudon-Padieu, E. (2008). Ultrastructural detection of an unusual intranuclear bacterium in Pentastiridius leporinus (Hemiptera: Cixiidae). J. Invertebr. Path., 97, 310 313.
3. Arnold, A.E. Lewis, L.C. (2005). Ecology and evolution of fungal endophytes and their roles against insects. In : Insect-Fungal Associations: Ecology and Evolution (eds Blackwell, M. Vega, F.E.). Oxford University Press, Oxford, pp. 211 243.
4. Ba, A.S., Guo, D.A., Norton, R.A., Phillips, S.A. Nes, W.D. (1995). Developmental differences in the sterol composition of Solenopsis invicta. Arch. Insect Biochem., 29, 1 9.
5. Bammert, G.F. Fostel, J.M. (2000). Genome-wide expression patterns in Saccharomyces cerevisiae: comparison of drug treatments and genetic alterations affecting biosynthesis of ergosterol. Antimicrob. Agents Chemother., 44, 1255 1265.
6. de Bary, A. (1879). The Phenomenon of Symbiosis. Karl J. Trubner, Strasbourg.
7. Brues, C.T. Glaser, R.W. (1921). A symbiotic fungus occurring in the fat-body of Pulvinaria innumerabilis Rath. Biol. Bull., 40, 299 U10.
8. Buchner, P. (1965). Endosymbiosis of Animals with Plant Microorganisms. Interscience, New York.
9. Bull, J.J. (1983). Evolution of Sex Determining Mechanisms. Benjamin/Cummings Publishing Co., Inc., Menlo Park.
10. Cardoza, Y.J., Klepzig, K.D. Raffa, K.F. (2006). Bacteria in oral secretions of an endophytic insect inhibit antagonistic fungi. Ecol. Entomol., 31, 636 645.
11. Cheng, D.J. Hou, R.F. (2001). Histological observations on transovarial transmission of a yeast-like symbiote in Nilaparvata lugens Stal (Homoptera: Delphacidae). Tissue Cell, 33, 273 279.
12. Dale, C., Plague, G.R., Wang, B., Ochman, H. Moran, N.A. (2002). Type III secretion systems and the evolution of mutualistic endosymbiosis. Proc. Natl. Acad. Sci. USA, 99, 12397 12402.
13. Deacon, J. (2006). Fungal Biology. Wiley-Blackwell, New York.
14. Degnan, P.H., Lazarus, A.B. Wernegreen, J.J. (2005). Genome sequence of Blochmannia pennsylvanicus indicates parallel evolutionary trends among bacterial mutualists of insects. Genome Res., 15, 1023 1033.
15. Dillon, R.J. Dillon, V.M. (2004). The gut bacteria of insects: nonpathogenic interactions. Annu. Rev. Entomol., 49, 71 92.
16. von Dohlen, C.D., Kohler, S., Alsop, S.T. McManus, W.R. (2001). Mealybug beta-proteobacterial endosymbionts contain gamma-proteobacterial symbionts. Nature, 412, 433 436.
17. Douglas, A.E. (2007). Symbiotic microorganisms: untapped resources for insect pest control. Trends Biotechnol., 25, 338 342.
18. Douglas, A.E. (2008). Conflict, cheats and the persistence of symbioses. New Phytol., 177, 849 858.
19. Douglas, A.E. (2009). The microbial dimension in insect nutritional ecology. Funct. Ecol., 23, 38 47.
20. Dujon, B., Sherman, D., Fischer, G., Durrens, P., Casaregola, S. Lafontaine, I. (2004). Genome evolution in yeasts. Nature, 430, 35 44.
21. Ebbert, M.A., Marlowe, J.L. Burkholder, J.J. (2003). Protozoan and intracellular fungal gut endosymbionts in Drosophila: prevalence and fitness effects of single and dual infections. J. Invertebr. Path., 83, 37 45.
22. Fermaud, M. Lemenn, R. (1992). Transmission of Botrytis cinerea to grapes by Grape Berry Moth larvae. Phytopathology, 82, 1393 1398.
23. Fukatsu, T. Ishikawa, H. (1996). Phylogenetic position of yeast-like symbiont of Hamiltonaphis styraci (Homoptera: Aphididae) based on 18S rDNA sequence. Insect Biochem. Mol. Biol., 26, 383 388.
24. Gibson, C.M. Hunter, M.S. (2005). Reconsideration of the role of yeasts associated with Chrysoperla green lacewings. Biol. Control, 32, 57 64.
25. Gibson, C.M. Hunter, M.S. (2009a). Inherited fungal and bacterial endosymbionts of a parasitic wasp and its cockroach host. Microb. Ecol., 57, 542 549.
26. Gibson, C.M. Hunter, M.S. (2009b). Negative fitness consequences and transmission dynamics of a heritable fungal symbiont of a parasitic wasp. Appl. Environ. Microbiol., 75, 3115 3119.
27. Gil, R., Silva, F.J., Zientz, E., Delmotte, F., Gonzalez-Candelas, F., Latorre, A. et al. (2003). The genome sequence of Blochmannia floridanus: comparative analysis of reduced genomes. Proc. Natl. Acad. Sci. USA, 100, 9388 9393.
28. Gusteleva, L.A. (1975). Biosynthesis of vitamins of B group by yeasts symbiotic on xylophagous insects. Microbiology, 44, 36 38.
29. Harrington, T.C. (2005). Ecology and evolution of mycophagous bark beetles and their fungal partners. In : Insect-Fungal Associations: Ecology and Evolution (eds Blackwell, M. Vega, F.E.). Oxford University Press, Oxford, pp. 211 243.
30. Heritage, J., Evans, E.G.V. Killington, R.A. (1996). Introductory Microbiology. Cambridge University Press, New York.
31. Hilgenboecker, K., Hammerstein, P., Schlattmann, P., Telschow, A. Werren, J.H. (2008). How many species are infected with Wolbachia? A statistical analysis of current data. FEMS Microbiol. Lett., 281, 215 220.
32. Hogg, S. (2005). Essential Microbiology. John Wiley and Sons, Ltd., San Francisco.
33. Hongoh, Y. Ishikawa, H. (2000). Evolutionary studies on uricases of fungal endosymbionts of aphids and planthoppers. J. Mol. Evol., 51, 265 277.
34. Jackson, R.W. (2009). Plant Pathogenic Bacteria: Genomics and Molecular Biology. Caister Academic Press, Norfolk, UK.
35. Jones, K.G. (1981). Baldcypress allelochemicals and the inhibition of silkworm enteric microorganisms: some ecological considerations. J. Chem. Ecol., 7, 103 114.
36. Jurzitza, G. (1966). Das wachstum normaler und aposymbiontischer Lasioderma serricorne F (Coleoptera: Anobiidae) bei suboptimaler caseindosierung. Naturwissenschaften, 53, 709 716.
37. Jurzitza, G. (1969). Vitamin requirements of normal and aposymbiotic Lasioderma serricorne F (Coleoptera: Anobiidae) and role of symbiotic fungi as vitamin sources for their hosts. Oecologia, 3, 70 75.
38. Keeling, P.J. Slamovits, C.H. (2004). Simplicity and complexity of microsporidian genomes. Eukaryot. Cell, 3, 1363 1369.
39. Kikuchi, Y., Hosokawa, T. 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.
40. Klepzig, K.D., Adams, A.S., Handelsman, J. Raffa, K.F. (2009). Symbioses: a key driver of insect physiological processes, ecological interactions, evolutionary diversification, and impacts on humans. Environ. Entomol., 38, 67 77.
41. Kumamoto, C.A. Vinces, M.D. (2005). Alternative Candida albicans lifestyles: growth on surfaces. Annu. Rev. Microbiol., 59, 113 133.
42. Labandeira, C. (2007). The origin of herbivory on land: initial patterns of plant tissue consumption by arthropods. Insect Sci., 14, 259 275.
43. Lemos, E.G.D., Alves, L.M.C. Campanharo, J.C. (2003). Genomics-based design of defined growth media for the plant pathogen Xylella fastidiosa. FEMS Microbiol. Lett., 219, 39 45.
44. Lushbaugh, W.B., Rowton, E.D. McGhee, R.B. (1976). Redescription of Coccidiascus legeri Chatton, 1913 (Nematosporaceae: Hemiascomycetidae), an intracellular parasitic yeastlike fungus from intestinal epithelium of Drosophila melanogaster. J. Invertebr. Path., 28, 93 107.
45. Mahadav, A., Gerling, D., Gottlieb, Y., Czosnek, H. Ghanim, M. (2008). Parasitization by the wasp Eretmocerus mundus induces transcription of genes related to immune response and symbiotic bacteria proliferation in the whitefly Bemisia tabaci. BMC Genomics, 9, 342.
46. Martin, M.M. Kukor, J.J. (1984). Role of mycophagy and bacteriophagy in invertebrate nutrition. In : Current Perspectives in Microbial Ecology (eds Klug, M.J. Reddy, C.A.). American Society for Microbiology, Washington, DC. 257 263.
47. McCreadie, J.W., Beard, C.E. Adler, P.H. (2005). Context-dependent symbiosis between black flies (Diptera: Simuliidae) and trichomycete fungi (Harpellales: Legeriomycetaceae). Oikos, 108, 362 370.
48. Miller, T.A. (2008). Pest and disease challenges and insect biotechnology solutions. Entomol. Res., 38, 34 40.
49. Moran, N.A., Tran, P. Gerardo, N.M. (2005). Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl. Environ. Microbiol., 71, 8802 8810.
50. Moran, N.A., McCutcheon, J.P. Nakabachi, A. (2008). Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet., 42, 165 190.
51. Murray, R.G.E. Schleifer, K.H. (1994). Taxonomic notes - a proposal for recording the properties of putative taxa of prokaryotes. Int. J. Syst. Bacteriol., 44, 174 176.
52. Nardi, J.B., Mackie, R.I. Dawson, J.O. (2002). Could microbial symbionts of arthropod guts contribute significantly to nitrogen fixation in terrestrial ecosystems? J. Insect Physiol., 48, 751 763.
53. Nardon, P. Grenier, A.M. (1989). Endosymbiosis in Coleoptera: biological, biochemical, and genetic aspects. In : Insect Endocytobiosis: Morphology, Physiology, Genetics, Evolution (eds Schwemmler, W. Gassner, G.). CRC Press, Boca Raton, pp. 175 216.
54. Nguyen, N.H., Suh, S.O. Blackwell, M. (2007). Five novel Candida species in insect-associated yeast clades isolated from Neuroptera and other insects. Mycologia, 99, 842 858.
55. Noda, H. Kawahara, N. (1995). Electrophoretic karyotype of intracellular yeast-like symbiotes in rice planthoppers and anobiid beetles. J. Invertebr. Path., 65, 118 124.
56. Noda, H. Kodama, K. (1996). Phylogenetic position of yeastlike endosymbionts of anobiid beetles. Appl. Environ. Microbiol., 62, 162 167.
57. Noda, H. Koizumi, Y. (2003). Sterol biosynthesis by symbiotes: cytochrome P450 sterol C-22 desaturase genes from yeastlike symbiotes of rice planthoppers and anobiid beetles. Insect Biochem. Mol. Biol., 33, 649 658.
58. Olsen, L.E. Hoy, M.A. (2002). Heat curing Metaseiulus occidentalis (Nesbitt) (Acari: Phytoseiidae) of a fitness-reducing microsporidium. J. Invertebr. Path., 79, 173 178.
59. Pant, N.C., Gupta, P. Nayar, J.K. (1960). Physiology of intracellular symbiotes of Stegobium paniceum L with special reference to amino acid requirements of the host. Experientia, 16, 311 312.
60. Perez-Brocal, V., Gil, R., Ramos, S., Lamelas, A., Postigo, M., Michelena, J.M. et al. (2006). Small microbial genome: the end of a long symbiotic relationship? Science, 314, 312 313.
61. Phaff, H.J. Starmer, W.T. (1987). Yeasts associated with plants, insects and soil. In : The Yeasts (eds Rose, A.H. Harrison, J.S.). Academic, New York, 123 180.
62. Reiman, D.A. (2008). 'Til death do us part': coming to terms with symbiotic relationships. Nat. Rev. Microbiol., 6, 721 724.
63. Sasaki, T., Kawamura, M. Ishikawa, H. (1996). Nitrogen recycling in the brown planthopper, Nilaparvata lugens: involvement of yeast-like endosymbionts in uric acid metabolism. J. Insect Physiol., 42, 125 129.
64. Scannell, D.R., Butler, G. Wolfe, K.H. (2007). Yeast genome evolution - the origin of the species. Yeast, 24, 929 942.
65. Shen, S.K. Dowd, P.F. (1992). Detoxifying enzymes and insect symbionts. J. Chem. Educ., 69, 796 799.
66. Slippers, B., Coutinho, T.A., Wingfield, B.D. Wingfield, M.J. (2003). A review of the genus Amylostereum and its association with woodwasps. S. Afr. J. Sci., 99, 70 74.
67. Srutka, P., Pazoutova, S. Kolarik, M. (2007). Daldinia decipiens and Entonaema cinnabarina as fungal symbionts of Xiphydria wood wasps. Mycol. Res., 111, 224 231.
68. Suh, S.O. Blackwell, M. (2004). Three new beetle-associated yeast species in the Pichia guilliermondii clade. FEMS Yeast Res., 5, 87 95.
69. Suh, S.O., Noda, H. Blackwell, M. (2001). Insect symbiosis: derivation of yeast-like endosymbionts within an entomopathogenic filamentous lineage. Mol. Biol. Evol., 18, 995 1000.
70. Suh, S.O., McHugh, J.V., Pollock, D.D. Blackwell, M. (2005). The beetle gut: a hyperdiverse source of novel yeasts. Mycol. Res., 109, 261 265.
71. Sung, G.H., Poinar, G.O. Spatafora, J.W. (2008). The oldest fossil evidence of animal parasitism by fungi supports a Cretaceous diversification of fungal-arthropod symbioses. Mol. Phylogenet. Evol., 49, 495 502.
72. Vega, F.E. (2008). Insect pathology and fungal endophytes. J. Invertebr. Pathol., 98, 277 279.
73. Vega, F.E. Dowd, P.F. (2005). The role of yeasts as insect endosymbionts. In : Insect-Fungal Associations: Ecology and Evolution (eds Blackwell, M. Vega, F.E.). Oxford University Press, Oxford, pp. 211 243.
74. Vega, F.E., Blackburn, M.B., Kurtzman, C.P. Dowd, P.F. (2003). Identification of a coffee berry borer-associated yeast: does it break down caffeine? Entomol. Exp. Appl., 107, 19 24.
75. Vishniac, H.S. Johnson, D.T. (1990). Development of a yeast flora in the adult green June beetle (Cotinis nitida, Scarabaeidae). Mycologia, 82, 471 479.
76. Willey, J., Sherwood, L. Woolverton, C. (2007). Microbiology. McGraw-Hill Science/Engineering/Math, New York.
77. Wren, H.N. Cochran, D.G. (1987). Xanthine dehydrogenase activity in the cockroach endosymbiont Blattabacterium cuenoti (Mercier 1906) Hollande and Favre 1931 and in the cockroach fat body. Comp. Biochem. Phys. B, 88, 1023 1026.
78. Yoshida, N., Oeda, K., Watanabe, E., Mikami, T., Fukita, Y., Nishimura, K. et al. (2001). Protein function - chaperonin turned insect toxin. Nature, 411, 44 45.
79. Zacchi, I. Vaughn-Martini, A. (2002). Yeasts associated with insects in agricultural areas of Perugia, Italy. Annu. Rev. Microbiol., 52, 237 244.
80. Zhang, N., Suh, S.O. Blackwell, M. (2003). Microorganisms in the gut of beetles: evidence from molecular cloning. J. Invertebr. Path., 84, 226 233.