Chapter 19 : Invertebrates—Insects

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in

Invertebrates—Insects, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817770/9781555812676_Chap19-1.gif /docserver/preview/fulltext/10.1128/9781555817770/9781555812676_Chap19-2.gif


Insects (phylum Arthropoda; class Insecta) are one of the most diverse groups of living creatures on Earth. One salient theme to emerge from early investigations was that distinct microbial symbionts, or communities of microbial symbionts, were especially common in insects that feed on restricted and/or relatively refractory food resources. Accordingly, a major challenge in preparing this chapter has been to distill the enormous body of literature on insect-microbe interactions into a coherent and meaningful overview. To do this, the author has often cited other reviews as a gateway to background literature on a particular topic, opting to focus here on some exciting recent discoveries, especially those in which biochemical, genetic, and molecular biological approaches have greatly improved our understanding of the symbioses and their evolution. The chapter emphasizes the biodiversity of the interacting partners and to suggest systems in which bioprospecting for novel and useful natural products, genes, enzymes, or organisms might be fruitful. The intracellular symbionts can be divided into two general groups based on their pattern of interaction with various insects and the effect they exert on their host: (i) the Wolbachia group, which induce reproductive anomalies in their hosts and may be regarded as parasites and (ii) the primary (bacteriocyte-associated) and secondary endosymbionts, which usually have beneficial or neutral effects on host fitness. Ectosymbionts of insects include a wide array of bacteria, yeast, and filamentous fungi. The chapter focuses primarily on recent discoveries made in studies of fungus-cultivating ants, fungus-cultivating termites, and ambrosia and bark beetles.

Citation: Breznak J. 2004. Invertebrates—Insects, p 191-203. In Bull A (ed), Microbial Diversity and Bioprospecting. ASM Press, Washington, DC. doi: 10.1128/9781555817770.ch19

Key Concept Ranking

Type III Secretion System
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

(A) Diversity of prokaryotic microbes located on and near the hindgut epithelium (GT) of the termite , (B) Cells of within an aphid bacteriocyte (kindly supplied by P. Baumann). Bars: (A) 1 µm; (B) 5 µm.

Citation: Breznak J. 2004. Invertebrates—Insects, p 191-203. In Bull A (ed), Microbial Diversity and Bioprospecting. ASM Press, Washington, DC. doi: 10.1128/9781555817770.ch19
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Akman, L.,, and S. Aksoy. 2001. A novel application of gene arrays: Escherichia coli array provides insight into the biology of the obligate endosymbiont of tsetse flies. Proc. Nat. Acad. Sci. USA 98:75467551.
2. Akman, L.,, R. V. M. Rio,, C. B. Beard,, and S. Aksoy. 2001. Genome size determination and coding capacity of Sodalis glossinidius, an enteric symbiont of tsetse flies, as revealed by hybridization to Escherichia coli gene arrays. J. Bacteriol. 183:45174525.
3. Akman, L.,, A. Yamashita,, H. Watanabe,, K. Oshima,, T. Shiba,, M. Hattori,, and S. Aksoy. 2002. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat. Genet. 32:402407.
4. Aksoy, S. 1995. Wigglesworthia gen. nov. and Wigglesworthia glossinidia sp. nov., taxa consisting of the mycetocyte-associated, primary endosymbionts of tsetse flies. Int. J. Syst. Bacteriol. 45:848851.
5. Amann, R. 2000. Who is out there? Microbial aspects of biodiversity. Syst. Appl. Microbiol. 23:18.
6. Anderson, J. M.,, A. D. M. Rayner,, and D. W. H. Walton. 1984. Invertebrate-Microbial Interactions. Cambridge University Press, Cambridge, United Kingdom.
7. Bandi, C.,, G. Damiani,, L. Magrassi,, A. Grigolo,, R. Fani,, and L. Sacchi. 1994. Flavobacteria as intracellular symbionts in cockroaches. Proc. R. Soc. Lond. Sci. 257:4348.
8. Bandi, C.,, M. Sironi,, G. Damiani,, L. Magrassi,, C. A. Nalepa,, U. Landani,, and L. Sacchi. 1995. The establishment of intracellular symbiosis in an ancestor of cockroaches and termites. Proc. R. Soc. Lond. Sci. B 259:293299.
9. Baumann, P.,, N. A. Moran,, and L. Baumann,. 2002. Bacteriocyte-associated endosymbionts of insects. In M. Dworkin (éd.), The Prokaryotes (on-line version). Springer-Verlag, New York, N.Y..
10. Bayon, C. 1980. Volatile fatty acids and methane production in relation to anaerobic carbohydrate fermentation in Oryctes nasicornis larvae (Coleoptera: Scarabaeidae). J. Insect. Physiol. 26:819828.
11. Beard, C. B.,, C. Cordon-Rosales,, and R. V. Durvasula. 2002. Bacterial symbionts of the Triatominae and their potential use in control of Chagas disease. Annu. Rev. Entomol. 47:123141.
12. Beaver, R. A., 1989. Insect-fungus relationships in the bark and ambrosia beetles, p. 121143. In N. Wilding,, N. M. Collins,, P. M. Hammond,, and J. F. Webber (ed.), Insect-Fungus Interactions. Academic Press, London, United Kingdom.
13. Breznak, J. A., 2000. Ecology of prokaryotic microbes in the guts of wood-and litter-feeding termites, p. 209231. In T. Abe,, D. E. Bignell,, and M. Higashi (ed.), Termites: Evolution, Sociality, Symbiosis, Ecology. Kluwer Academic, Dordrecht, The Netherlands.
14. Breznak, J. A. 2002. Phylogenetic diversity and physiology of termite hindgut spirochetes. Integ. Comp. Biol. 42:313318.
15. Breznak, J. A.,, and J. R. Leadbetter,. 2002. Termite gut spirochetes. In M. Dworkin (éd.), The Prokaryotes. [Online.] Springer-Verlag, New York, N.Y..
16. Brune, A., 2003. Symbionts aiding digestion, p. 11021107. In V. H. Resh, and R. T. Cardé (ed.), Encyclopedia of Insects. Academic Press, Inc., New York, N.Y..
17. Brune, A.,, D. Emerson,, and J. A. Breznak. 1995. The termite gut microflora as an oxygen sink: microelectrode determination of oxygen and pH gradients in guts of lower and higher termites. Appl. Environ. Microbiol. 61:26812687.
18. Buchner, P. 1965. Endosymbiosis of Animals with Plant Microorganisms. John Wiley & Sons, Inc., New York, N.Y..
19. Cassar, S.,, and M. Blackwell. 1996. Convergent origins of ambrosia fungi. Mycologia 88:596601.
20. Cazemier, A. E.,, H. J. M. OpdenCamp,, J. H. P. Hackstein,, and G. D. Vogels. 1997. Fibre digestion in arthropods. Comp. Biochem. Physiol. A 118:101109.
21. Chapela, I. H.,, S. A. Rehner,, T. R. Schultz,, and U. G. Mueller. 1994. Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science 266:16911694.
22. Chen, X. A.,, S. Li,, and S. Aksoy. 1999. Concordant evolution of a symbiont with its host insect species: molecular phylogeny of genus Glossina and its bacteriome-associated endosymbiont, Wigglesworthia glossinidia. J. Mol. Evol. 48:4958.
23. Clark, J. W.,, S. Hossain,, C. R. Burnside,, and S. Kambhampati. 2001a. Coevolution between a cockroach and its bacterial endosymbiont: a biogeographical perspective. Proc. R. Soc. Lond. Ser. B 268:393398.
24. Clark, M. A.,, L. Baumann,, M. L. L. Thao,, N. A. Moran,, and P. Baumann. 2001b. Degenerative minimalism in the genome of a psyllid endosymbiont. J. Bacteriol. 183:18531861.
25. Costa, H. S.,, D. E. Ulmann,, M. W. Johnson,, and B. E. Tabashnik. 1993. Antibiotic oxtetracycline interferes with Bemisia tabaci (Homoptera, Aleyrodidae) oviposition, development, and ability to induce squash silverleaf. Ann. Entomol, Soc. Am. 86: 740748.
26. Costa, H. S.,, N. C. Toscano,, and T. J. Henneyberry. 1996. Mycetocyte inclusion in the oocytes of Bemisia argentifolii (Homoptera: Aleyrodidae). Ann. Entomol. Soc. Am. 89:694699.
27. Costa, H. S.,, T. J. Henneberry,, and N. C. Toscano. 1997. Effects of antibacterial materials on Bemisia argentifolii (Homoptera: Aleyrodidae) oviposition, growth, survival, and sex ratio. J. Econ. Entomol. 90:333339.
28. Currie, C. R. 2001. A community of ants, fungi, and bacteria: a multilateral approach to studying symbiosis. Annu. Rev. Microbiol. 55:357380.
29. Currie, C. R.,, J. A. Scott,, R. C. Summerbell,, and D. Malloch. 1999. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398:701704.
30. Dale C.,, and I. Maudlin. 1999. Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans. Int. J. Syst. Bacteriol. 49:267275.
31. Dale, C.,, S. A. Young,, D. T. Haydon,, and S. C. Welburn. 2001. The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc. Natl. Acad. Sci. USA 98:18831888.
32. Dale, C.,, G. R. Plague,, B. Wang,, H. Ochman,, and N. A. Moran. 2002. Type III secretion systems and the evolution of mutualistic endosymbiosis. Proc. Natl. Acad. Sci. USA 99:1239712402.
33. Dasch, G. A.,, E. Weiss,, and K. P. Chang,. 1984. B. Endosymbionts of insects, p. 811833. In N. R. Krieg,, and J. G. Holt (ed.), Bergey's Manual of Systematic Bacteriology. Williams & Wilkins, Baltimore, Md.
34. de Bary, A. 1879 Die Erscheinung der Symbiose. Trubner, Strassburg, Austria.
35. Dillon, R.,, and K. Charnley. 2002. Mutualism between the desert locust Schistocerca gregaria and its gut microbiota. Res. Microbiol. 153:503509.
36. Douglas, A. E. 1989. Mycetocyte symbiosis in insects. Biol. Rev. 64:409434.
37. Douglas, A. E., 1992. Symbiotic microorganisms in insects, pp. 165178. In J. Lederberg (ed.), Encyclopedia of Microbiology. Academic Press, Inc., San Diego, Calif..
38. Dowd, P. F. 1992. Insect fungal symbionts: a promising source of detoxifying enzymes. J. Ind. Microbiol. 9:149161.
39. Drew, R. A. I.,, and A. C. Lloyd,. 1991. Bacteria in the life cycle of tephritid fruit flies, p. 441465. In P. Barbosa,, V. A. Krischik,, and C. G. Jones (ed.), Microbial Mediation of Plant-Herbivore Interactions. John Wiley & Sons, Inc., New York, N.Y.
40. Eggleton, P. 2001. Termites and trees: a review of recent advances in termite phylogenetics. Insectes Sociaux 48:187193.
41. Farrell, B. D.,, A. S. Sequeira,, B. C. O'Meara,, B. B. Normark,, J. H. Chung,, and B. H. Jordal. 2001. The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55:20112027.
42. Friedrich, M. W.,, D. Schmitt-Wagner,, T. Lueders,, and A. Brune. 2001. Axial differences in community structure of Crenarchaeota and Euryarchaeota in the highly compartmentalized gut of the soil-feeding termite Cubitermes orthognathus. Appl. Environ. Microbiol. 67:48804890.
43. Galan, J. E.,, and A. Collmer. 1999. Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284:13221328.
44. Gebhardt, K., et al. 2002. Screening for biologically active metabolites with endosymbiotic bacilli isolated from arthropods. FEMS Lett. 217:199205.
45. Gherna, R. L.,, J. H. Werren,, W. Weisburg,, R. Cote,, C. R. Woese,, L. Mandeico,, and D. J. Brenner. 1991. Arsenophonus nasoniae gen. nov., sp.nov., the causative agent of the son-killer trait in the parasitic wasp Nasonia vitripennis. Int. J. Syst. Bacteriol. 41:563565.
46. Gijzen, H. J.,, C. A. M. Broers,, M. Barughare,, and C. K. Stumm. 1991. Methanogenic bacteria as endosymbionts of the ciliate Nyctotherus ovalis in the cockroach hindgut. Appl. Environ. Microbiol. 57:16301634.
47. Gijzen, H. J.,, C. van der Drift,, M. Bamgahare,, and H. J. M. op den Camp. 1994. Effect of host diet and hindgut microbial composition on cellulolytic activity in the hindgut of the American cockroach, Periplaneta americana. Appl. Environ. Microbiol. 60:18221826.
48. Hackett, K. J.,, D. E. Lynn,, D. L. Williamson,, A. S. Ginsberg,, and R. F. Whitcomb. 1986. Cultivation of the Drosophila sex-ratio Spiroplasma. Science 232:12531255.
49. Hackstein, J. H. P.,, and C. K. Stumm. 1994. Methane production in terrestrial arthropods. Proc. Natl. Acad. Sci. USA 91:54415445.
50. Hinkle, G.,, J. K. Wetterer,, T. R. Schultz,, and M. L. Sogin. 1994. Phylogeny of the attine ant fungi based on analysis of small subunit ribosomal RNA gene sequences. Science 266:16951697.
51. Hölldobler, B.,, and E. O. Wilson. 1990. The Ants. Belknap Press, Cambridge, Mass.
52. Howard, D. J.,, G. L. Bush,, and J. A. Breznak. 1985. The evolutionary significance of bacteria associated with Rhagoletis. Evolution 39:405417.
53. Hugenholtz, P.,, B. M. Goebel,, and N. R. Pace. 1998. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J. Bacteriol. 180:47654774.
54. Hurst, G. D. D.,, T. C. Hammarton,, C. Bandi,, T. M. O. Majerus,, D. Bertrand,, and M. E. N. Majerus. 1997. The diversity of inherited parasites of insects: the male-killing agent of the ladybird beetle Coleomegilla maculata is a member of the Flavobacteria. Genet. Res. 70:16.
55. Hypsa, V.,, and C. Dale. 1997. In vitro culture and phylogenetic analysis of "Candidatus Arsenophonus triatominarum," an intracellular bacterium from the triatomine bug, Triatoma infestans. Int.J. Syst. Bacteriol. 47:11401144.
56. Iida, T.,, M. Ohkuma,, K. Ohtoko,, and T. Kudo. 2000. Symbiotic spirochetes in the termite hindgut: phylogenetic identification of ectosymbiotic spirochetes of oxymonad protists. FEMS Microbiol. Ecol. 34:1726.
57. Inoue, T.,, O. Kitade,, T. Yoshimura,, and I. Yamaoka,. 2000. Symbiotic associations with protists, p. 275288. In T. Abe,, D. E. Bignell,, and M. Higashi (éd.), Termites: Evolution, Sociality, Symbioses, Ecology. Kluwer Academic Publishers, Dordrecht, The Netherlands.
58. Jeyaprakash, A.,, and M. A. Hoy. 2000. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol. Biol. 9:393405.
59. Jones, K. G.,, and M. Blackwell. 1998. Phylogenetic analysis of ambrosia species in the genus Raffaelea based on 18S rDNA sequences. Mycol. Res. 102:661665.
60. Kane, M. D., 1997. Microbial fermentation in insect guts, pp. 231265. In R. I. Mackie,, and B. A. White (éd.), Gastrointestinal Microbiology. Chapman & Hall, New York, N.Y.
61. Kane, M. D.,, and N. E. Pierce,. 1994. Diversity within diversity: molecular approaches to studying microbial interactions with insects, p. 509524. In B. Schierwater,, B. Streit,, G. Wagner,, and R. DeSalle (éd.), Molecular Methods in Ecology and Evolution. Birkhauser Verlag, Berlin, Germany.
62. Katoh, H.,, T. Miura,, K. Maekawa,, N. Shinzato,, and T. Matsumoto. 2002. Genetic variation of symbiotic fungi cultivated by the macrotermitine termite Odontoternes formosanus (Isoptera: Termitidae) in the Ryukyu Archipelago. Mol. Ecol. 11:15651572.
63. Kaufman, M. G.,, and M. J. Klug. 1991. The contribution of hindgut bacteria to dietary carbohydrate utilization by crickets (Orthoptera: Gryllidae). Comp. Biochem. Physiol. 98:117123.
64. Kaufman, M. G.,, M. J. Klug,, and R. W. Merritt. 1989. Growth and food utilization parameters of germ-free house crickets, Acheta domesticus. J. Insect Physiol. 35:957967.
65. Kaufman, M. G.,, E. D. Walker,, D. A. Odelson,, and M. J. Klug. 2000. Microbial community ecology and insect nutrition. Am. Entomol. 46:173184.
66. Komaki, K.,, and H. Ishikawa. 1999. Intracellular bacterial symbionts of aphids posess many genomic copies per bacterium. J. Mol. Evol. 48:717722.
67. Lauzon, C. R.,, R. E. Sjogren,, and R. J. Prokopy. 2000. Enzymatic capabilities of bacteria associated with apple maggot flies: a postulated role in attraction. J. Chem. Ecol. 26:953967.
68. Leadbetter, J. R.,, and J. A. Breznak. 1996. Physiological ecology of Methanobrevibacter cuticularis sp. nov. and Methanobrevibacter curvatus sp. nov., isolated from the hindgut of the termite Reticulitermes flavipes. Appl. Environ. Microbiol. 62:36203631.
69. Leadbetter, J. R.,, L. D. Crosby,, and J. A. Breznak. 1998. Methanobrevibacter filiformis sp. nov., a filamentous methanogen from termite hindguts. Arch. Microbiol. 169:287292.
70. Leadbetter, J. R.,, T. M. Schmidt,, J. R. Graber,, and J. A. Breznak. 1999. Acetogenesis from H2 plus C02 by spirochetes from termite guts. Science 283:686689.
71. Lilburn, T. G.,, T. M. Schmidt,, and J. A. Breznak. 1999. Phylogenetic diversity of termite gut spirochaetes. Environ. Microbiol. 1:331345.
72. Lilburn, T. G.,, K. S. Kim,, N. E. Ostrom,, K. R. Byzek,, J. R. Leadbetter,, and J. A. Breznak. 2001. Nitrogen fixation by symbiotic and free-living spirochetes. Science 292:24952498.
73. Martin, M. M. 1987. Invertebrate-Microbial Interactions: Ingested Fungal Enzymes in Arthropod Biology. Comstock Publishing Associates, Ithaca, N.Y.
74. Moran, N. A.,, and P. Baumann. 2000. Bacterial endosymbionts in animals. Curr. Opin. Microbiol. 3:270275.
75. Moran, N. A.,, C. Dale,, H. Dunbar,, W.A. Smith,, and H. Ochman. 2003. Intracellular symbionts of sharpshooters (Insecta: Hemiptera: Cicadellinae) form a distinct clade with a small genome. Environ. Microbiol. 5:116126.
76. Nalepa, C. A.,, and C. Bandi,. 2000. Characterizing the ancestors: paedomorphosis and termite evolution, p. 5373. In T. Abe,, D. E. Bignell,, and M. Higashi (éd.), Termites: Evolution, Sociality, Symbioses, Ecology. Kluwer Academic Publishers, Dordrecht, The Netherlands.
77. Nalepa, C.,, G. Byers,, C. Bandi,, and M. Sironi. 1997. Description of Cryptocercus clevelandi (Dictyoptera: Cryptocercidae) from the northwestern United States, molecular analysis of bacterial symbionts in its fat body, and notes on biology, distribution, and biogeography. Ann. Entomol. Soc. Am. 90:416424.
78. Novotny, V.,, Y. Basset,, S. E. Miller,, G. W. Weiblen,, B. Bremer,, L. Cizek,, and P. Drozd. 2002. Low host specificity of herbivorous insects in a tropical forest. Nature 416:841844.
79. Ohkuma, M.,, and T. Kudo. 1996. Phylogenetic diversity of the intestinal bacterial community in the termite Reticulitermes speratus. Appl. Environ. Microbiol. 62:461468.
80. Ohkuma, M.,, and T. Kudo. 1998. Phylogenetic analysis of the symbiotic intestinal microflora of the termite Cryptotermes domesticus. FEMS Microbiol. Lett. 164:389395.
81. Ohkuma, M.,, S. Noda,, Y. Hongoh,, and T. Kudo. 2002. Diverse bacteria related to the Bacteroides subgroup of the CFB phylum within the gut symbiotic communities of various termites. Biosci. Biotechnol. Biochem. 66:7884.
82. Ohtoko, K.,, M. Ohkuma,, S. Moriya,, T. Inoue,, R. Usami,, and T. Kudo. 2000. Diverse genes of cellulase homologues of glycosyl hydrolase family 45 from the symbiotic protists in the hindgut of the termite Reticulitermes speratus. Extremophiles 4:343349.
83. O'Neill, S. L.,, A. A. Hoffmann,, and J. H. Werren (ed). 1997. Influential Passengers. Oxford University Press, Oxford, United Kingdom.
84. Polver, P. P. D.,, L. Sacchi,, L. Cima,, A. Grigolo,, and U. Laudani. 1986. Oxidoreductase distribution in the fat body and symbionts of the German cockroach Blatella germánica: a histochemical approach. Cell. Mol. Biol. 32:701708.
85. Paine, T. D.,, K. F. Raffa,, and T. C. Harrington. 1997. Interactions among scolytid bark beetles, their associated fungi, and live host conifers. Annu. Rev. Entomol. 42:179206.
86. Pimm, S. L.,, G. J. Russell,, J. L. Gittleman,, and T. M. Brooks. 1995. Future of biodiversity. Science 269:347350.
87. Rouland-Lèfevre, C. 2000. Symbiosis with fungi, p. 289306. In T. Abe,, D. E. Bignell,, and M. Higashi (éd.), Termites: Evolution, Sociality, Symbioses, Ecology. Kluwer Academic Publishers, Dordrecht, The Netherlands.
88. Rouland-Lefevre, C.,, N. M. Diouf,, A. Brauman,, and M. Neyra. 2002. Phylogenetic relationships in I (family Agaricaceae) based on the nucleotide sequence of ITS: a first approach to elucidate the evolutionary history of the symbiosis between fungus-growing termites and their fungi. Mol. Phylogenet. Evol. 22:423429.
89. Sanderson, M. G. 1996. Biomass of termites and their emissions of methane and carbon dioxide: a global database. Global Biogeochem. Cycles 10:543557.
90. Sandstrom, J. P.,, J. A. Russell,, J. P. White,, and N. A. Moran. 2001. Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol. Ecol. 10:217228.
91. Sauer, C.,, E. Stackebrandt,, J. Gadau,, B. Holldobler,, and R. Gross. 2000. Systematic relationships and cospeciation of bacterial endosymbionts and their carpenter ant host species: proposal of the new taxon Candidatus Blochmannia gen. nov. Int. J. Syst. Evol. Microbiol. 50:18771886.
92. Sauer, C.,, D. Dudaczek,, B. Holldobler,, and R. Gross. 2002. Tissue localization of the endosymbiotic bacterium "Candidatus Blochmannia floridanus" in adults and larvae of the carpenter ant Camponotus floridanus. Appl. Environ. Microbiol. 68: 41874193.
93. Smith, D. C.,, and A. E. Douglas. 1987. The Biology of Symbiosis. Edward Arnold, London, United Kingdom.
94. Sprenger, W. W.,, M. C. van Belzen,, J. Rosenberg,, J. H. P. Hackstein,, and J. T. Keltjens. 2000. Methanomicrococcus blatticola gen. nov., sp. nov., a methanol- and methylamine-reducing methanogen from the hindgut of the cockroach Periplaneta americana. Int. J. Syst. Evol. Microbiol. 50:19891999.
95. Stackebrandt, E.,, and B. M. Goebel. 1994. Taxonomie note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int. J. Syst. Bacteriol. 44:846849.
96. Staley, J. T.,, and A. Konopka. 1985. Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu. Rev. Microbiol. 39:321346.
97. Stouthamer, R.,, J. A. J. Breeuwer,, and G. D. D. Hurst. 1999. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu. Rev. Microbiol. 53:71102.
98. Subandiyah, S.,, N. Nikoh,, S. Tsuyumu,, S. Somowiyarjo,, and T. Fukatsu. 2000. Complex endosymbiotic microbiota of the citrus psyllid Diaphorina citri (Homoptera: Psylloidea). Zool. Set. 17:983989.
99. Sugimoto, A.,, D. E. Bignell,, and J. A. MacDonald,. 2000. Global impact of termites on the carbon cycle and atmospheric trace gases, p. 409435. In T. Abe,, D. E. Bignell,, and M. Higashi (ed.), Termites: Evolution, Sociality, Symbioses, Ecology. Kluwer Academic Publishers, Dordrecht, The Netherlands.
100. Tamas, I.,, L. Klasson,, B. Canbàck,, A. K. Nàslund,, A.-S. Eriksson,, J. J. Wernegreen,, J. P. Sandstrom,, N. A. Moran,, and S. G. E. Andersson. 2002. 50 Million years of genomic stasis in endosymbiotic bacteria. Science 296:23762379.
101. Taprab, Y.,, M. Ohkuma,, T. Johjima,, Y. Maeda,, S. Moriya,, T. Inoue,, P. Suwanarit,, N. Noparatnaraporn,, and T. Kudo. 2002. Molecular phylogeny of symbiotic basidiomycetes of fungus-growing termites in Thailand and their relationship with the host. Biosci. Biotecbnol. Biochem. 66: 11591163.
102. Thao, M. L. L.,, N. A. Moran,, P. Abbot,, E. B. Brennan,, D. H. Burckhardt,, P. Baumann. 2000. Cospeciation of psyllids and their primary prokaryotic endosymbionts. Appl. Environ. Microbiol. 66:28982905.
103. Thao, M. L. L.,, P. J. Gullan,, and P. Baumann. 2002. Secondary (γ -Proteobacteria) endosymbionts infect the primary (β -Proteobacteria) endosymbionts of mealybugs multiple times and coevolve with their hosts. Appl. Environ. Microbiol. 68: 31903197.
104. Tokuda, G.,, N. Lo,, H. Watanabe,, M. Slaytor,, T. Matsumoto,, and H. Noda. 1999. Metazoan cellulase genes from termites: intron/exon structures and sites of expression. Biochim. Biophys. Acta 1447:146159.
105. Tokuda, G.,, I. Yamaoka,, and H. Noda. 2000. Localization of symbiotic clostridia in the mixed segment of the termite Nasutitermes takasagoensis (Shiraki). Appl. Environ. Microbiol. 66:21992207.
106. Tsuchida, T.,, R. Koga,, H. Shibao,, T. Matsumoto,, and T. Fukatsu. 2002. Diversity and geographic distribution of secondary enä-dosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum. Mol. Ecol. 11:21232135.
107. von Dohlen, C. D.,, S. Kohier,, S. T. Alsop,, and W. R. McManus. 2001. Mealybug β -proteobacterial endosymbionts contain γ -proteobacterial symbionts. Nature 412:433436.
108. Wernegreen, J. J. 2002. Genome evolution in bacterial endosymbionts of insects. Nat. Rev. Genet. 3:850861.
109. Werren, J.,, G. Hurst,, W. Zhang,, W. J. Breeuwer,, R. Stouthamer,, and M. Majerus. 1994. Rickettsial relative associated with male killing in the ladybird beetle (Adalia bipunctata). J. Bacteriol. 176:388394.
110. Werren, J. H.,, D. Windsor,, and L. Guo. 1995. Distribution of Wolbachia among neotropical arthropods. Proc. R. Soc. Lond. Ser. B 262:197204.
111. Wilson, E. O. 1992. The Diversity of Life. W. W. Norton & Company, New York, N.Y.
112. Wren, H. N.,, and D. G. Cochran. 1987. Xanthine dehydrogenase activity in the cockroach endosymbiont Blattabacterium cuenoti (Mercier 1906) Hollande and Favre 1931 and in the cockroach fat body. Comp. Biochem. Physiol. 88:10231026.
113. Yamin, M. 1979. Flagellates of the orders Trichomonadida Kirby, Oxymonadida Grasse, and Hypermastigida Grassi & Foà reported from lower termites (Isoptera families Mastotermitidae, Hodotermitidae, Termopsidae, Rhinotermitidae, and Serritermitidae) and from the wood-feeding roach Cryptocercus (Dictyoptera: Cryptocercidae). Sociobiology 4:1119.


Generic image for table
Table 1

Distribution of primary (P) and secondary (S) endosymbionts in insects

Citation: Breznak J. 2004. Invertebrates—Insects, p 191-203. In Bull A (ed), Microbial Diversity and Bioprospecting. ASM Press, Washington, DC. doi: 10.1128/9781555817770.ch19

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error