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The Prokaryotes pp 465–496Cite as

Bacteriocyte-Associated Endosymbionts of Insects

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Abstract

Intracellular associations between bacteria and insects are widespread in nature (Baumann and Moran 1997; Buchner 1965; Dasch et al. 1984; Douglas 1989; Houk and Griffiths 1980). Extensive studies of the natural history of such associations have led to the conclusion that they are commonly found in insects that utilize diets containing an excess of one class of compounds but a deficiency of some essential nutrients (Buchner 1965; Dadd 1985). It was thought that the function of the endosymbionts was to rectify this imbalance by the synthesis of these essential nutrients for the host. Extensive compilations of the occurrence of endosymbionts in different groups of insects are found in Buchner (1965) and Dasch et al. (1984). Because most of the prokaryotes involved in such associations are not cultivable on common laboratory media, their characterization had to await the development of recombinant DNA methodology. The past 10 years have witnessed the initiation of studies on the intracellular association of prokaryotes with a variety of insect hosts. In this chapter, we will provide an overview of the evolution and, where possible, genetics and physiology of such recently studied associations. A summary of some of their features is presented in Table 19.1, and the phylogeny of the endosymbionts based on 16S rDNA is presented in Fig. 19.1.

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References

  • Akhtar S, van Emden HF (1994) Ultrastructure of the symbionts and mycetocytes of bird cherry aphid (Rhopalosiphum padi). Tissue Cell 26:513–522

    CAS  PubMed  Google Scholar 

  • Aksoy S (1995a) Molecular analysis of the endosymbionts of tsetse flies: 16S rDNA locus and over-expression of a chaperonin. Insect Mol Biol 4:23–29

    CAS  PubMed  Google Scholar 

  • Aksoy S (1995b) Wigglesworthia gen. nov. and Wigglesworthia glossinidia sp. nov., taxa consisting of the mycetocyte-associated, primary endosymbionts of tsetse flies. Int J Syst Bacteriol 45:848–851

    CAS  PubMed  Google Scholar 

  • Aksoy S, Pourhosseini AA, Chow A (1995) Mycetome endosymbionts of tsetse flies constitute a distinct lineage related to the Enterobacteriaceae. Insect Mol Biol 4:15–22

    CAS  PubMed  Google Scholar 

  • Aksoy S, Chen X, Hypsa V (1997) Phylogeny and potential transmission routes of midgut-associated endosymbionts of tsetse (Diptera: Glossinidae). Insect Mol Biol 6:183–190

    CAS  PubMed  Google Scholar 

  • Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169

    CAS  PubMed  Google Scholar 

  • Andersson SGE, Zomorodipour A, Andersson JO, Sicheritz-Ponten T, Alsmark UCM, Podowski RM, Naslund AK, Eriksson AS, Winkler HH, Kurland CG (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133–140

    CAS  PubMed  Google Scholar 

  • Baker JE (1975) Vitamin requirements of larvae of Sitophilus oryzae. J Insect Physiol 21:1337–1342

    CAS  Google Scholar 

  • Baker JE (1979) Requirements for the essential dietary amino acids of larvae of the rice weevil. Environ Entomol 8:451–453

    CAS  Google Scholar 

  • Baker JE, Lum PTM (1973) Development of aposymbiosis in larvae of Sitophilus oryzae by dietary treatment with antibiotics. J Stored Prod Res 9:241–245

    CAS  Google Scholar 

  • Bandi C, Damiani G, Magrassi L, Grigolo A, Fani R, Sacchi L (1994) Flavobacteria as intracellular symbionts in cockroaches. Proc R Soc Lond B Biol Sci 257:43–48

    CAS  Google Scholar 

  • Bandi C, Sironi M, Damiani G, Magrassi L, Nalepa CA, Laudani U, Sacchi L (1995) The establishment of intracellular symbiosis in an ancestor of cockroaches and termites. Proc R Soc Lond B Biol Sci 259:293–299

    CAS  Google Scholar 

  • Bandi C, Sironi M, Nalepa CA, Corona S, Sacchi L (1997) Phylogenetically distant intracellular symbionts in termites. Parassitologia 39:71–75

    CAS  PubMed  Google Scholar 

  • Bandi C, Anderson TJC, Genchi C, Blaxter ML (1998) Phylogeny of Wolbachia in filarial nematodes. Proc R Soc Lond B Biol Sci 265:2407–2414

    CAS  Google Scholar 

  • Bandi C, McCall JW, Genchi C, Corona S, Venco L, Sacchi L (1999) Effects of tetracycline on the filarial worms Brugia pahangi and Dirofilaria immitis and their bacterial endosymbionts Wolbachia. Int J Parasitol 29:357–364

    CAS  PubMed  Google Scholar 

  • Bandi C, Sacchi L. Intracellular symbiosis. In: Abe T, Higashi M, Bignel D (eds) Termites: their symbiosis, behavior, and global diversification. Kluwer, Dordrecht (in press)

    Google Scholar 

  • Barancin CE, Smoot JC, Findlay RH, Actis LA (1998) Plasmid-mediated histamine biosynthesis in the bacterial fish pathogen Vibrio anguillarum. Plasmid 39:235–244

    CAS  PubMed  Google Scholar 

  • Baumann L, Baumann P (1994) Growth kinetics of the endosymbiont Buchnera aphidicola in the aphid Schizaphis graminum. Appl Environ Microbiol 60:3440–3443

    CAS  PubMed  Google Scholar 

  • Baumann L, Baumann P (1998) Characterization of ftsZ, the cell division gene of Buchnera aphidicola (endosymbiont of aphids) and detection of the product. Curr Microbiol 36:85–89

    CAS  PubMed  Google Scholar 

  • Baumann P, Moran NA (1997) Non-cultivable microorganisms from symbiotic associations of insects and other hosts. Antonie Van Leeuwenhoek 72:39–48

    CAS  PubMed  Google Scholar 

  • Baumann P, Baumann L, Lai CY, Roubakhsh D, Moran NA, Clark MA (1995) Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu Rev Microbiol 49:55–94

    CAS  PubMed  Google Scholar 

  • Baumann P, Baumann L, Clark MA (1996) Levels of Buchnera aphidicola chaperonin GroEL during growth of the aphid Schizaphis graminum. Curr Microbiol 32:279–285

    CAS  Google Scholar 

  • Baumann P, Moran NA, Baumann L (1997a) The evolution and genetics of aphid endosymbionts. Bioscience 47:12–20

    Google Scholar 

  • Baumann L, Clark MA, Rouhbakhsh D, Baumann P, Moran NA, Voegtlin DJ (1997b) Endosymbionts (Buchnera) of the aphid Uroleucon sonchi contain plasmids with trpEG and remnants of trpE pseudogenes. Curr Microbiol 35:18–21

    CAS  Google Scholar 

  • Baumann L, Baumann P, Moran NA (1998a) The endosymbiont (Buchnera) of the aphid Diuraphis noxia contains all the genes of the tryptophan biosynthetic pathway. Curr Microbiol 37:58–59

    CAS  PubMed  Google Scholar 

  • Baumann P, Baumann L, Clark MA, Thao ML (1998b) Buchnera aphidicola: the endosymbiont of aphids. ASM News 64:203–209

    Google Scholar 

  • Baumann L, Baumann P, Thao ML (1999a) Detection of messenger RNA transcribed from genes encoding enzymes of amino acid biosynthesis in Buchnera aphidicola (endosymbiont of aphids). Curr Microbiol 38:135–136

    CAS  PubMed  Google Scholar 

  • Baumann L, Baumann P, Moran MA, Sandström J, Thao ML (1999b) Genetic characterization of plasmids containing genes encoding enzymes of leucine biosynthesis in endosymbionts (Buchnera) of aphids. J Mol Evol 48:77–85

    CAS  PubMed  Google Scholar 

  • Beard CB, O’Neill SL, Tesh RB, Richards FF, Aksoy S (1993a) Modification of arthropod vector competence via symbiotic bacteria. Parasitol Today 9:179–183

    CAS  PubMed  Google Scholar 

  • Beard CB, O’Neill SK, Mason P, Mandelco L, Woese CR, Tesh RB, Richards FF, Aksoy S (1993b) Genetic transformation and phylogeny of bacterial symbionts from tsetse. Insect Mol Biol 1:123–131

    CAS  PubMed  Google Scholar 

  • Bensaadi-Merchermek N, Salvado JC, Cagnon C, Karama S, Mouches C (1995) Characterization of the unlinked 16S rDNA and 23S-5S rRNA operon of Wolbachia pipientis, a prokaryotic parasite of insect gonads. Gene 165:81–86

    CAS  PubMed  Google Scholar 

  • Berlyn MKB (1998) Linkage map of Escherichia coli K-12, edition 10: the traditional map. Microbiol Mol Biol Rev 62:814–984

    CAS  PubMed  Google Scholar 

  • Bigliardi E, Selmi MG, Corona S, Bandi CA, Sacchi L (1995) Membrane systems in endocytobiosis. III. Ultrastructural features of symbionts and vacuolar membrane in bacteriocytes of the wood-eating cockroach Cryptocercus punctulatus (Dictyoptera, Cryptocercidae). Boll Zool 62:235–238

    Google Scholar 

  • Blackman RL (1984) Reproduction, cytogenetics and development. In: Minks AK, Harrewijn P (eds) Aphids: their biology, natural enemies and control, vol 2A. Elsevier Biomedical Press, Amsterdam, pp 163–195

    Google Scholar 

  • Blackman RL, Eastop VF (1984) Aphids on the world’s crops. Wiley, Chichester, UK

    Google Scholar 

  • Blattner FR, Plunkett G, Bloch CA, Perna NT, Burland V, Riley M, ColladoVides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y (1997) The complete genome sequence of Escherichia coli K-12. Science 277:1453–1462

    CAS  PubMed  Google Scholar 

  • Blua MJ, Perring TM, Madore MA (1994) Plant virus-induced changes in aphid population development and temporal fluctuations in plant nutrients. J Chem Ecol 20:691–707

    CAS  Google Scholar 

  • Boman HG, Hultmark D (1987) Cell-free immunity in insects. Annu Rev Microbiol 41:103–126

    CAS  PubMed  Google Scholar 

  • Borror DJ, Triplehorn CA, Johnson NF (1989) An introduction to the study of insects. Harcourt Brace College, Fort Worth

    Google Scholar 

  • Bracho AM, Martínez-Torres D, Moya A, Latorre A (1995) Discovery and molecular characterization of a plasmid localized in Buchnera sp., bacterial endosymbiont of the aphid Rhopalosiphum padi. J Mol Evol 41:67–73

    CAS  PubMed  Google Scholar 

  • Brenner DJ (1984) Enterobacteriaceae. In: Krieg NR, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 1. Williams and Wilkins, Baltimore, pp 408–506

    Google Scholar 

  • Brough CN, Dixon AFG (1990) Ultrastructural features of egg development in oviparae of vetch aphid, Megoura viciae. Tissue Cell 22:51–63

    CAS  PubMed  Google Scholar 

  • Brown JK, Frohlich DR, Rosell RC (1995) The sweetpotato or silverleaf whiteflies—biotypes of Bemisia tabaci or a species complex. Annu Rev Entomol 40:511–534

    CAS  Google Scholar 

  • Brynnel EU, Kurland CG, Moran NA, Andersson SGE (1998) Evolutionary rates for tuf genes in endosymbionts of aphids. Mol Biol Evol 15:574–582

    CAS  PubMed  Google Scholar 

  • Buchner P (1965) Endosymbiosis of animals with plant microorganisms. Interscience, New York

    Google Scholar 

  • Campbell BC, Bragg TS, Turner CE (1992) Phylogeny of symbiotic bacteria of four weevil species (Coleoptera, Curculionidae) based on analysis of 16S ribosomal DNA. Insect Biochem Mol Biol 22:415–421

    CAS  Google Scholar 

  • Campbell BC, Stefen-Campbell JD, Gill RJ (1994) Evolutionary origin of whiteflies (Hemiptera: Sternorrhyncha: Aleyrodidae) inferred from 18S rDNA sequences. Insect Mol Biol 3:73–88

    CAS  PubMed  Google Scholar 

  • Chang KP, Musgrave AJ (1969) Histochemistry and ultrastructure of the mycetome and its “symbiotes” in the pear psylla, Psylla pyricola Foerster (Homoptera). Tissue Cell 1:597–606

    CAS  PubMed  Google Scholar 

  • Charles H, Ishikawa H (1999) Physical and genetic map of the genome of Buchnera, the primary endosymbiont of the pea aphid Acyrthosiphon pisum. J Mol Evol 48:142–150

    CAS  PubMed  Google Scholar 

  • Charles H, Ishikawa H, Nardon P (1995) Presence of a protein specific of endocytobiosis (symbionin) in the weevil Sitophilus. C R Acad Sci Paris Ser III 318:35–41

    CAS  Google Scholar 

  • Charles H, Condemine G, Nardon C, Nardon P (1997a) Genome size characterization of the principal endocellular symbiotic bacteria of the weevil Sitophilus oryzae, using pulsed field gel electrophoresis. Insect Biochem Mol Biol 27:345–350

    CAS  Google Scholar 

  • Charles H, Heddi A, Guillaud J, Nardon C, Nardon P (1997b) A molecular aspect of symbiotic interactions between the weevil Sitophilus oryzae and its endosymbiotic bacteria: over-expression of a chaperonin. Biochem Biophys Res Commun 239:769–774

    CAS  PubMed  Google Scholar 

  • Chen D-Q, Purcell AH (1997) Occurrence and transmission of facultative endosymbionts in aphids. Curr Microbiol 34:220–225

    CAS  PubMed  Google Scholar 

  • Chen DQ, Campbell BC, Purcell AH (1996) A new rickettsia from a herbivorous insect, the pea aphid Acyrthosiphon pisum (Harris). Curr Microbiol 33:123–128

    CAS  PubMed  Google Scholar 

  • Chen XA, Li S, Aksoy S (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 48:49–58

    CAS  PubMed  Google Scholar 

  • Cheng Q, Aksoy S (1999) Tissue tropism, transmission and expression of foreign genes in vivo in midgut symbionts of tsetse flies. Insect Mol Biol 8:125–132

    CAS  PubMed  Google Scholar 

  • Clark MA, Baumann L, Munson MA, Baumann P, Campbell BC, Duffus JE, Osborne LS, Moran NA (1992) The eubacterial endosymbionts of whiteflies (Homoptera, Aleyrodoidea) constitute a lineage distinct from the endosymbionts of aphids and mealybugs. Curr Microbiol 25:119–123

    Google Scholar 

  • Clark MA, Baumann L, Baumann P, Rouhbakhsh D (1996) Ribosomal protein S1(RpsA) of Buchnera aphidicola, the endosymbiont of aphids: characterization of the gene and detection of the product. Curr Microbiol 32:89–94

    CAS  PubMed  Google Scholar 

  • Clark MA, Baumann L, Baumann P (1998a) Sequence analysis of a 34.7-kb DNA segment from the genome of Buchnera aphidicola (endosymbiont of aphids) containing groEL, dnaA, the atp operon, gidA, and rho. Curr Microbiol 36:158–163

    CAS  PubMed  Google Scholar 

  • Clark MA, Baumann L, Baumann P (1998b) Buchnera aphidicola (aphid endosymbiont) contains genes encoding enzymes of histidine biosynthesis. Curr Microbiol 37:356–358

    CAS  PubMed  Google Scholar 

  • Clark MA, Baumann P, Moran MA (1999a) Buchnera plasmid-associated trpEG probably originated from a chromosomal location between hslU and fpr. Curr Microbiol 38:309–311

    CAS  Google Scholar 

  • Clark MA, Moran NA, Baumann P (1999b) Sequence evolution in bacterial endosymbionts having extreme base compositions. Mol Biol Evol 16:1586–1598

    CAS  PubMed  Google Scholar 

  • Clark MA, Moran NA, Baumann P (2000) Cospeciation between bacterial endosymbionts (Buchnera) and a recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution 54(2):517–525

    CAS  PubMed  Google Scholar 

  • Cochoran DG (1985) Nitrogen excretion in cockroaches. Annu Rev Entomol 30:29–49

    Google Scholar 

  • Costa HS, Ullman DE, Johnson MW, Tabashnik BE (1993a) Antibiotic oxytetracycline interferes with Bemisia tabaci (Homoptera, Aleyrodidae) oviposition, development, and ability to induce squash silverleaf. Ann Entomol Soc Am 86:740–748

    CAS  Google Scholar 

  • Costa HS, Westcot DM, Ullman DE, Johnson MW (1993b) Ultrastructure of the endosymbionts of the whitefly, Bemisia tabaci and Trialeurodes vaporariorum. Protoplasma 176:106–115

    Google Scholar 

  • Costa HS, Westcot DM, Ullman DE, Rosell R, Brown JK, Johnson MW (1995) Morphological variation in Bemisia endosymbionts. Protoplasma 189:194–202

    Google Scholar 

  • Costa HS, Toscano NC, Henneberry TJ (1996) Mycetocyte inclusion in the oocytes of Bemisia argentifolii (Homoptera, Aleyrodidae). Ann Entomol Soc Am 89:694–699

    Google Scholar 

  • Costa HS, Henneberry TJ, Toscano NC (1997) Effects of antibacterial materials on Bemisia argentifolii (Homoptera: Aleyrodidae) oviposition, growth, survival, and sex ratio. J Econ Entomol 90:333–339

    CAS  Google Scholar 

  • Crawford IP (1989) Evolution of a biosynthetic pathway—the tryptophan paradigm. Annu Rev Microbiol 43:567–600

    CAS  PubMed  Google Scholar 

  • Dadd RH (1985) Nutrition: organisms. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry, and pharmacology, vol 4. Pergamon, Elmsford, pp 315–319

    Google Scholar 

  • Dale C, Maudlin I (1999) Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans. Int J Syst Bacteriol 49:267–275

    CAS  PubMed  Google Scholar 

  • Dasch GA (1975) Morphological and molecular studies on intracellular bacterial symbiotes of insects. Yale University, New Haven

    Google Scholar 

  • Dasch GA, Weiss E, Chang K-P (1984) Endosymbionts of insects. In: Krieg NR, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 1. Williams and Wilkins, Baltimore, pp 811–833

    Google Scholar 

  • Denk D, Böck A (1987) l-Cysteine biosynthesis in Escherichia coli: nucleotide sequence and expression of the serine acetyltransferase (cysE) gene from wild-type and a cysteine-excreting mutant. J Gen Microbiol 133:515–525

    CAS  PubMed  Google Scholar 

  • Dixon AFG (1973) Biology of aphids. Edward Arnold, London

    Google Scholar 

  • Dixon AFG (1992) Constraints on the rate of parthenogenetic reproduction and pest status of aphid. Invertebr Reprod Dev 22:159–163

    Google Scholar 

  • Douglas AE (1988) Sulfate utilization in an aphid symbiosis. Insect Biochem 18:159–163

    Google Scholar 

  • Douglas AE (1989) Mycetocyte symbiosis in insects. Biol Rev Camb Philos Soc 64:409–434

    CAS  PubMed  Google Scholar 

  • Douglas AE (1990) Nutritional interactions between Myzus persicae and its symbionts. In: Campbell RK, Eikenbary RD (eds) Aphid-plant genotype interactions. Elsevier Biomedical Press, Amsterdam, pp 319–327

    Google Scholar 

  • Douglas AE (1997) Parallels and contrasts between symbiotic bacteria and bacterial-derived organelles: evidence from Buchnera, the bacterial symbiont of aphids. FEMS Microbiol Ecol 24:1–9

    CAS  Google Scholar 

  • Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37

    CAS  PubMed  Google Scholar 

  • Douglas AE, Dixon AFG (1987) The mycetocyte symbiosis of aphids: variation with age and morph in virginoparae of Megoura viciae and Acyrthosiphon pisum. J Insect Physiol 33:109–113

    Google Scholar 

  • Douglas AE, Prosser WA (1992) Synthesis of the essential amino acid tryptophan in the pea aphid (Acyrthosiphon pisum) symbiosis. J Insect Physiol 38:565–568

    CAS  Google Scholar 

  • Douglas AE, Smith DC (1989) Are endosymbioses mutualistic? Trends Ecol Evol 4:350–352

    CAS  PubMed  Google Scholar 

  • Durvasula RV, Gumbs A, Panackal A, Kruglov O, Aksoy S, Merrifield RB, Richards FF, Beard CB (1997) Prevention of insect-borne disease: an approach using transgenic symbiotic bacteria. Proc Natl Acad Sci USA 94:3274–3278

    CAS  PubMed  Google Scholar 

  • Eisen JA (1995) The RecA Protein as a model molecule for molecular systematic studies of bacteria—comparison of trees of RecAs and 16S rRNAs from the same species. J Mol Evol 41:1105–1123

    CAS  PubMed  Google Scholar 

  • Eremeeva ME, Ching WM, Wu YL, Silverman DJ, Dasch GA (1998) Western blotting analysis of heat shock proteins of Rickettsiales and other eubacteria. FEMS Microbiol Lett 167:229–237

    CAS  PubMed  Google Scholar 

  • Faye I (1978) Insect immunity: early fate of bacteria injected in a Saturniid pupae. J Invertebr Pathol 31:19–26

    Google Scholar 

  • Filichkin SA, Brumfield S, Filichkin TP, Young MJ (1997) In vitro interactions of the aphid endosymbiotic SymL chaperonin with barley yellow dwarf virus. J Virol 71:569–577

    CAS  PubMed  Google Scholar 

  • Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, Kerlavage AR, Bult CJ, Tomb JF, Dougherty BA, Merrick JM, McKenney K, Sutton G, Fitzhugh W, Fields C, Gocayne JD, Scott J, Shirley R, Liu LI, Glodek A, Kelley JM, Weidman JF, Phillips CA, Spriggs T, Hedblom E, Cotton MD, Utterback TR, Hanna MC, Nguyen DT, Saudek DM, Brandon RC, Fine LD, Fritchman JL, Fuhrmann JL, Geoghagen NSM, Gnehm CL, McDonald LA, Small KV, Fraser CM, Smith HO, Venter JC (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:469–512

    Google Scholar 

  • Forrest JMS (1987) Galling aphids. In: Minks AK, Harrewijn P (eds) Aphids: their biology, natural enemies and control, vol 2A. Elsevier, Amsterdam, pp 341–353

    Google Scholar 

  • Fraser CM, Gocayne JD, White O, Adams MD, Clayton RA, Fleischmann RD, Bult CJ, Kerlavage AR, Sutton G, Kelley JM, Fritchman JL, Weidman JF, Small KV, Sandusky M, Fuhrmann J, Nguyen D, Utterback TR, Saudek DM, Phillips CA, Merrick JM, Tomb JF, Dougherty BA, Bott KF, Hu PC, Lucier TS, Peterson SN, Smith HO, Hutchison CA, Venter JC (1995) The minimal gene complement of Mycoplasma genitalium. Science 270:397–403

    CAS  PubMed  Google Scholar 

  • Fraser CM, Casjens S, Huang WM, Sutton GG, Clayton R, Lathigra R, White O, Ketchum KA, Dodson R, Hickey EK, Gwinn M, Dougherty B, Tomb JF, Fleischmann RD, Richardson D, Peterson J, Kerlavage AR, Quackenbush J, Salzberg S, Hanson M, vanVugt R, Palmer N, Adams MD, Gocayne J, Weidman J, Utterback T, Watthey L, McDonald L, Artiach P, Bowman C, Garland S, Fujii C, Cotton MD, Horst K, Roberts K, Hatch B, Smith HO, Venter JC (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580–586

    CAS  PubMed  Google Scholar 

  • Fukatsu T, Ishikawa H (1992a) A novel eukaryotic extracellular symbiont in an aphid, Astegopteryx styraci (Homoptera, Aphididae, Hormaphidinae). J Insect Physiol 38:765–773

    Google Scholar 

  • Fukatsu T, Ishikawa H (1992b) Soldier and male of an eusocial aphid Colophina arma lack endosymbiont: implications for physiological and evolutionary interaction between host and symbiont. J Insect Physiol 38:1033–1042

    Google Scholar 

  • Fukatsu T, Ishikawa H (1992c) Synthesis and localization of symbionin, an aphid endosymbiont protein. Insect Biochem Mol Biol 22:167–174

    CAS  Google Scholar 

  • Fukatsu T, Ishikawa H (1993) Occurrence of chaperonin-60 and chaperonin-10 in primary and secondary bacterial symbionts of aphids—implications for the evolution of an endosymbiotic system in aphids. J Mol Evol 36:568–577

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Fukatsu T, Ishikawa H (1998) Differential immunohistochemical visualization of the primary and secondary intracellular symbiotic bacteria of aphids. Appl Entomol Zool 33:321–326

    Google Scholar 

  • Fukatsu T, Nikoh N (1998) Two intracellular symbiotic bacteria from the mulberry psyllid Anomoneura mori (Insecta, Homoptera). Appl Environ Microbiol 64:3599–3606

    CAS  PubMed  Google Scholar 

  • Fukatsu T, Aoki S, Kurosu U, Ishikawa H (1994) Phylogeny of Cerataphidini aphids revealed by their symbiotic microorganisms and basic structure of their galls: implications for host-symbiont coevolution and evolution of sterile soldier castes. Zool Sci 11:613–623

    Google Scholar 

  • Fukatsu T, Watanabe K, Sekiguchi Y (1998) Specific detection of intracellular symbiotic bacteria of aphids by oligonucleotide-probed in situ hybridization. Appl Entomol Zool 33:461–472

    Google Scholar 

  • Gasnier-Fauchet F, Nardon P (1986) Comparison of methionine metabolism in symbiotic and aposymbiotic larvae of Sitophilus oryzae L. (Coleoptera: curculionidae). II. Involvement of the symbiotic bacteria in the oxidation of methionine. Comp Biochem Physiol 85B:251–254

    CAS  Google Scholar 

  • Gasnier-Fauchet F, Gharib A, Nardon P (1986) Comparison of methionine metabolism in symbiotic and aposymbiotic larvae of Sitophilus oryzae L. (Coleoptera: Curculionidae) I. Evidence for a glycine N-methyltransferase-like activity in the aposymbiotic larvae. Comp Biochem Physiol 85B:245–250

    CAS  Google Scholar 

  • Gray SM, Banerjee N (1999) Mechanisms of arthropod transmission of plant and animal viruses. Microbiol Mol Biol Rev 63:128–148

    CAS  PubMed  Google Scholar 

  • Grenier AM, Nardon C, Rahbe Y (1994) Observations on the micro-organisms occurring in the gut of the pea aphid Acyrthosiphon pisum. Entomol Exp Appl 70:91–96

    Google Scholar 

  • Griffiths GW, Beck SD (1973) Intracellular symbiotes of the pea aphid, Acyrthosiphon pisum. J Insect Physiol 19:75–84

    Google Scholar 

  • Griffiths GW, Beck SD (1974) Effect of antibiotics on intracellular symbiotes in the pea aphid, Acyrthosiphon pisum. Cell Tissue Res 148:287–300

    CAS  PubMed  Google Scholar 

  • Grinyer I, Musgrave AJ (1966) Ultrastructure and peripheral membranes of the mycetomal microorganism of Sitophilus granarius (L. coleoptera). J Cell Sci 1:181–186

    Google Scholar 

  • Gross CA (1996) Function and regulation of heat shock proteins. In: Neidhard FC (ed) Escherichia coli and Salmonella, vol 1. ASM Press, Washington, DC, pp 1382–1399

    Google Scholar 

  • Gross R, Rappuoli R (1988) Positive regulation of pertussis toxin expression. Proc Natl Acad Sci USA 85:3913–3917

    CAS  PubMed  Google Scholar 

  • Hara E, Ishikawa H (1990) Purification and partial characterization of symbionin, an aphid endosymbiont-specific protein. Insect Biochem 20:421–427

    CAS  Google Scholar 

  • Harada H, Ishikawa H (1993) Gut microbe of aphid closely related to its intracellular symbiont. Biosystems 31:185–191

    CAS  PubMed  Google Scholar 

  • Harada H, Oyaizu H, Ishikawa H (1996) A consideration about the origin of aphid intracellular symbiont in connection with gut bacterial flora. J Gen Appl Microbiol 42:17–26

    CAS  Google Scholar 

  • Harrison CP, Douglas AE, Dixon AFG (1989) A rapid method to isolate symbiotic bacteria from aphids. J Invertebr Pathol 53:427–428

    Google Scholar 

  • Harwood RF, James MT (1979) Entomology in human and animal health. Macmillan, New York

    Google Scholar 

  • Hassan AKM, Moriya S, Baumann P, Yoshikawa H, Ogasawara N (1996) Structure of the dnaA region of the endosymbiont, Buchnera aphidicola, of the aphid Schizaphis graminum. DNA Res 3:415–419

    CAS  PubMed  Google Scholar 

  • Heddi A, Lefebvre F, Nardon P (1991) The influence of symbiosis on the respiratory control ratio (RCR) and the ADP/O Ratio in the adult weevil-Sitophilus oryzae (Coleoptera, Curculionidae). Endocytobiosis Cell Res 8:61–73

    Google Scholar 

  • Heddi A, Lefebvre F, Nardon P (1993) Effect of endocytobiotic bacteria on mitochondrial enzymatic activities in the weevil Sitophilus oryzae (Coleoptera, Curculionidae). Insect Biochem Mol Biol 23:403–411

    CAS  Google Scholar 

  • Heddi A, Charles H, Khatchadourian C, Bonnot G, Nardon P (1998) Molecular characterization of the principal symbiotic bacteria of the weevil Sitophilus oryzae: a peculiar G–C content of an endocytobiotic DNA. J Mol Evol 47:52–61

    CAS  PubMed  Google Scholar 

  • Henry SM (1962) The significance of microorganisms in the nutrition of insects. Trans N Y Acad Sci 24:676–683

    CAS  Google Scholar 

  • Hinde R (1971a) The control of mycetome symbiotes of the aphids Brevicoryne brassicae, Myzus persicae, and Macrosiphon rosae. J Insect Physiol 17:1971–1800

    Google Scholar 

  • Hinde R (1971b) The fine structure of mycetome symbiotes of the aphids Brevicoryne brassicae, Myzus persicae, and Macrosiphum rosae. J Insect Physiol 17:2035–2050

    CAS  PubMed  Google Scholar 

  • Hogenhout SA, van derWilk F, Verbeek M, Goldbach RW, van den Heuvel JFJM (1998) Potato leafroll virus binds to the equatorial domain of the aphid endosymbiotic GroEL homolog. J Virol 72:358–365

    CAS  PubMed  Google Scholar 

  • Houk EJ, Griffiths GW (1980) Intracellular symbiotes of the Homoptera. Annu Rev Entomol 25:161–187

    CAS  Google Scholar 

  • Houk EJ, Griffiths GW, Hadjokas NE, Beck SD (1977) Peptidoglycan in the cell wall of the primary intracellular symbiote of the pea aphid. Science 198:401–403

    CAS  PubMed  Google Scholar 

  • Humphreys NJ, Douglas AE (1997) Partitioning of symbiotic bacteria between generations of insect: a quantitative study of a Buchnera sp. in the pea aphid (Acyrthosiphon pisum) reared at different temperatures. Appl Environ Microbiol 63:3294–3296

    CAS  PubMed  Google Scholar 

  • Iaccarino FM, Tremblay E (1973) Comparazione ultrastrutturale della disimbiosi di Macrosiphum rosae (L.) e Dactynotus jaceae (L.) (Homoptera, Aphididae). Boll Lab Entomol Agrar Filipo Silvestri 30:319–335

    Google Scholar 

  • Ishikawa H (1982) Isolation of the intracellular symbionts and partial characterizations of their RNA species of the elder aphid, Acyrthosiphon magnoliae. Comp Biochem Physiol 72B:239–247

    CAS  Google Scholar 

  • Ishikawa H (1987) Nucleotide composition and kinetic complexity of the genomic DNA of an intracellular symbiont in the pea aphid Acyrthosiphon pisum. J Mol Evol 24:205–211

    CAS  Google Scholar 

  • Kakeda K, Ishikawa H (1991) Molecular chaperon produced by an intracellular symbiont. J Biochem 110:583–587

    CAS  PubMed  Google Scholar 

  • Kambhampati S (1995) A phylogeny of cockroaches and related insects based on DNA sequence of mitochondrial ribosomal RNA genes. Proc Natl Acad Sci USA 92:2017–2020

    CAS  PubMed  Google Scholar 

  • Katsumata R, Ikeda M (1993) Hyperproduction of tryptophan in Corynebacterium glutamicum by pathway engineering. Biotechnology 11:921–925

    CAS  Google Scholar 

  • Klotz MG, Norton JM (1998) Multiple copies of ammonia monooxygenase (amo) operons have evolved under biased AT/GC mutational pressure in ammonia-oxidizing autotrophic bacteria. FEMS Microbiol Lett 168:303–311

    CAS  PubMed  Google Scholar 

  • Komaki K, Ishikawa H (1999) Intracellular symbionts of aphids are bacteria with numerous genomic copies. J Mol Evol 48:717–722

    CAS  PubMed  Google Scholar 

  • Kreditch NM (1996) Biosynthesis of cysteine. In: Neidhardt FC (ed) Escherichia coli and Salmonella, vol 1. ASM Press, Washington, DC, pp 514–527

    Google Scholar 

  • Kusano T, Takeshima T, Inoue C, Sugawara K (1991) Evidence for two sets of structural genes coding for ribulose bisphosphate carboxylase in Thiobacillus ferrooxidans. J Bacteriol 173:7313–7323

    CAS  PubMed  Google Scholar 

  • Lai CY, Baumann P (1992a) Genetic analysis of an aphid endosymbiont DNA fragment homologous to the rnpA-rpmH-dnaA-dnaN-gyrB region of eubacteria. Gene 113:175–181

    CAS  PubMed  Google Scholar 

  • Lai CY, Baumann P (1992b) Sequence analysis of a DNA fragment from Buchnera aphidicola (an endosymbiont of aphids) containing genes homologous to dnaG, rpoD, cysE andsecB. Gene 119:113–118

    CAS  PubMed  Google Scholar 

  • Lai CY, Baumann L, Baumann P (1994) Amplification of trpEG: adaptation of Buchnera aphidicola to an endosymbiotic association with aphids. Proc Natl Acad Sci USA 91:3819–3823

    CAS  PubMed  Google Scholar 

  • Lai C-Y, Baumann P, Moran NA (1995) Genetics of the tryptophan biosynthetic pathway of the prokaryotic endosymbiont (Buchnera) of the aphid Schlechtendalia chinensis. Insect Mol Biol 4:47–59

    CAS  PubMed  Google Scholar 

  • Lai CY, Baumann P, Moran N (1996) The endosymbiont (Buchnera sp.) of the aphid Diuraphis noxia contains plasmids consisting of trpEG and tandem repeats of trpEG pseudogenes. Appl Environ Microbiol 62:332–339

    CAS  PubMed  Google Scholar 

  • Lambert JD, Moran NA (1998) Deleterious mutations destabilize ribosomal RNA in endosymbiotic bacteria. Proc Natl Acad Sci USA 95:4458–4462

    CAS  PubMed  Google Scholar 

  • Liadouze I, Febvay G, Guillaud J, Bonnot G (1996) Metabolic fate of energetic amino acids in the aposymbiotic pea aphid Acyrthosiphon pisum (Harris) (Homoptera, Aphididae). Symbiosis 21:115–127

    CAS  Google Scholar 

  • Lipsitch M, Nowak MA, Ebert D, May RM (1995) The population dynamics of vertically and horizontally transmitted parasites. Proc R Soc Lond B Biol Sci 260:321–327

    CAS  Google Scholar 

  • Llanes C, Gabant P, Couturier M, Bayer L, Plesiat P (1996) Molecular analysis of the replication elements of the broad-host-range RepA/C replicon. Plasmid 36:26–35

    CAS  PubMed  Google Scholar 

  • Margolis N, Hogan D, Tilly K, Rosa PA (1994) Plasmid location of Borrelia purine biosynthesis gene homologs. J Bacteriol 176:6427–6432

    CAS  PubMed  Google Scholar 

  • Maynard Smith J, Szathmáry E (1995) The major transitions in evolution. W. H. Freeman Spektrum, Oxford/New York

    Google Scholar 

  • McLean DL, Houk EJ (1973) Phase contrast and electron microscopy pf the mycetocytes and symbiotes of the pea aphid, Acyrthosiphon pisum. J Insect Physiol 19:625–633

    Google Scholar 

  • McMillan DJ, Mau M, Walker MJ (1998) Characterisation of the urease gene cluster in Bordetella bronchiseptica. Gene 208:243–251

    CAS  PubMed  Google Scholar 

  • Messer W, Weigl C (1996) Initiation of chromosome replication. In: Neidhardt FC (ed) Escherichia coli and Salmonella, vol 2. ASM Press, Washington, DC, pp 1579–1601

    Google Scholar 

  • Moran NA (1996) Accelerated evolution and Muller’s ratchet in endosymbiotic bacteria. Proc Natl Acad Sci USA 93:2873–2878

    CAS  PubMed  Google Scholar 

  • Moran N, Baumann P (1994) Phylogenetics of cytoplasmically inherited microorganisms of arthropods. Trends Ecol Evol 9:15–20

    CAS  PubMed  Google Scholar 

  • Moran NA, Telang A (1998) Bacteriocyte-associated symbionts of insects: a variety of insect groups harbor ancient prokaryotic endosymbionts. Bioscience 48:295–304

    Google Scholar 

  • Moran NA, Munson MA, Baumann P, Ishikawa H (1993) A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc R Soc Lond B Biol Sci 253:167–171

    Google Scholar 

  • Moran NA, von Dohlen CD, Baumann P (1995) Faster evolutionary rates in endosymbiotic bacteria than in cospeciating insect hosts. J Mol Evol 41:727–731

    CAS  Google Scholar 

  • Moran NA, Kaplan ME, Gelsey MJ, Murphy TG, Scholes EA (1999) Phylogeny and evolution of the aphid genus Uroleucon based on nuclear and mitochondrial DNA sequences. Syst Entomol 24:85–93

    Google Scholar 

  • Munson MA, Baumann P, Kinsey MG (1991a) Buchnera gen. nov. and Buchnera aphidicola sp. nov., a taxon consisting of the mycetocyte-associated, primary endosymbionts of aphids. Int J Syst Bacteriol 41:566–568

    Google Scholar 

  • Munson MA, Baumann P, Clark MA, Baumann L, Moran NA, Voegtlin DJ, Campbell BC (1991b) Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J Bacteriol 173:6321–6324

    CAS  PubMed  Google Scholar 

  • Munson MA, Baumannn P, Moran MA (1992) Phylogenetic relationships of the endosymbionts of mealybugs (Homoptera: Pseudococcidae) based on 16S rDNA sequences. Mol Phylogenet Evol 1:26–30

    CAS  PubMed  Google Scholar 

  • Munson MA, Baumann L, Baumann P (1993) Buchnera aphidicola (a prokaryotic endosymbiont of aphids) contains a putative 16S rRNA operon unlinked to the 23S rRNA-encoding gene: sequence determination, and promoter and terminator analysis. Gene 137:171–178

    CAS  PubMed  Google Scholar 

  • Musgrave AJ, Grinyer I (1968) Membranes associated with the disintegration of mycetomal micro-organisms in Sitophilus zeamais (Mots. Coleoptera). J Cell Sci 3:65–70

    CAS  PubMed  Google Scholar 

  • Nakabachi A, Ishikawa H (1997) Differential display of mRNAs related to amino acid metabolism in the endosymbiotic system of aphids. Insect Biochem Mol Biol 27:1057–1062

    CAS  PubMed  Google Scholar 

  • Nakabachi A, Ishikawa H (1999) Provision of riboflavin to the host aphid, Acyrthosiphon pisum, by endosymbiotic bacteria, Buchnera. J Insect Physiol 45:1–6

    CAS  PubMed  Google Scholar 

  • Nardon P, Grenier AM (1988) Genetical and biochemical interactions between the host and its endocytobiotes in the weevil Sitophilus (Coleoptera, Curculionidae) and other related species. In: Scannerini S (ed) Cell to cell signals in plant, animal and microbial symbiosis. Springer, Heidelberg, pp 255–270

    Google Scholar 

  • Nicholson ML, Gaasenbeek M, Laudenbach DE (1995) Two enzymes together capable of cysteine biosynthesis are encoded on a cyanobacterial plasmid. Mol Gen Genet 247:623–632

    CAS  PubMed  Google Scholar 

  • Nogge G (1976) Aposymbiotic tsetse flies. Glossina morsitans morsitans obtained by feeding adults on rabbits immunized specifically with symbionts. J Insect Physiol 24:299–304

    Google Scholar 

  • Nogge G (1982) Significance of symbionts for the maintenance of an optimal nutritional state of successful reproduction in hematophagous arthropods. Parasitology 82:299–304

    Google Scholar 

  • Norton JM, Low JM, Martin G (1996) The gene encoding ammonia monooxygenase subunit A exists in three nearly identical copies in Nitrosospira sp. NpAV. FEMS Microbiol Lett 139:181–188

    CAS  PubMed  Google Scholar 

  • O’Neill A, Hoffman A, Werren JH (1997) Influential passengers; inherited microorganisms and arthropod reproduction. Oxford University Press, Oxford

    Google Scholar 

  • Ohtaka C, Nakamura H, Ishikawa H (1992) Structures of chaperonins from an intracellular symbiont and their functional expression in Escherichia coli groE mutants. J Bacteriol 174:1869–1874

    CAS  PubMed  Google Scholar 

  • Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220

    CAS  PubMed  Google Scholar 

  • Pennisi E (1998) Evolution—heat shock protein mutes genetic changes. Science 282:1796

    CAS  PubMed  Google Scholar 

  • Remaudière G, Remaudière M (1997) Catalogue des aphididae du monde. Institut National de la Recherche Agronomique, Paris

    Google Scholar 

  • Riley M, Labedan B (1996) Escherichia coli gene products: physiological functions and common ancestries. In: Neidhardt FC (ed) Escherichia coli and Salmonella, vol 2. ASM Press, Washington, DC, pp 2118–2202

    Google Scholar 

  • Romero D, Palacios R (1997) Gene amplification and genomic plasticity in prokaryotes. Annu Rev Genet 31:91–111

    CAS  PubMed  Google Scholar 

  • Roth JR, Benson N, Galitski T, Haack K, Lawrence JG, Miesel L (1996) Rearrangements of the bacterial chromosome: formation and applications. In: Neidhardt FC (ed) Escherichia coli and Salmonella, vol 2. ASM Press, Washington, DC, pp 2256–2276

    Google Scholar 

  • Rouhbakhsh D, Baumann P (1995) Characterization of a putative 23S-5S rRNA operon of Buchnera aphidicola (endosymbiont of aphids) unlinked to the 16S rRNA-encoding gene. Gene 155:107–112

    CAS  PubMed  Google Scholar 

  • Rouhbakhsh D, Moran NA, Baumann L, Voegtlin DJ, Baumann P (1994) Detection of Buchnera, the primary prokaryotic endosymbiont of aphids, using the polymerase chain reaction. Insect Mol Biol 3:213–217

    CAS  PubMed  Google Scholar 

  • Rouhbakhsh D, Lai CY, von Dohlen CD, Clark MA, Baumann L, Baumann P, Moran NA, Voegtlin DJ (1996) The tryptophan biosynthetic pathway of aphid endosymbionts (Buchnera): genetics and evolution of plasmid-associated anthranilate synthase (trpEG) within the Aphididae. J Mol Evol 42:414–421

    CAS  PubMed  Google Scholar 

  • Rouhbakhsh D, Clark MA, Baumann L, Moran NA, Baumann P (1997) Evolution of the tryptophan biosynthetic pathway in Buchnera (aphid endosymbionts): studies of plasmid-associated trpEG within the genus Uroleucon. Mol Phylogenet Evol 8:167–176

    CAS  PubMed  Google Scholar 

  • Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396:336–342

    CAS  PubMed  Google Scholar 

  • Sacchi L, Corona S, Grigolo A, Laudani U, Selmi MG, Bigliardi E (1996) The fate of the endocytobionts of Blattella germanica (Blattaria, Blattellidae) and Periplaneta americana (Blattaria, Blattidae) during embryo development. Ital J Zool 63:1–11

    Google Scholar 

  • Sacchi L, Nalepa CA, Bigliardi E, Corona S, Grigolo A, Laudani U, Bandi C (1998a) Ultrastructural studies of the fat body and bacterial endosymbionts of Cryptocercus punctulatus Scudder (Blattaria: Cryptocercidae). Symbiosis 25:251–269

    Google Scholar 

  • Sacchi L, Nalepa CA, Bigliardi E, Lenz M, Bandi C, Corona S, Grigolo A, Lambiase S, Laudani U (1998b) Some aspects of intracellular symbiosis during embryo development of Mastotermes darwiniensis (Isoptera: Mastotermitidae). Parassitologia 40:309–316

    CAS  PubMed  Google Scholar 

  • Sandström J, Moran N (1999) How nutritionally imbalanced is phloem sap for aphids? Entomol Exp Appl 91:203–210

    Google Scholar 

  • Sandström J, 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

    Google Scholar 

  • Sandström J, Telang A, Moran NA (2000) Nutritional enhancement of host plants by aphids-a comparison of three aphid species on grasses. J Insect Physiol 46:33–40

    PubMed  Google Scholar 

  • Sasaki T, Ishikawa H (1995) Production of essential amino acids from glutamate by mycetocyte symbionts of the pea aphid, Acyrthosiphon pisum. J Insect Physiol 41:41–46

    CAS  Google Scholar 

  • Sasaki T, Aoki T, Hayashi H, Ishikawa H (1990) Amino acid composition of the honeydew of symbiotic and aposymbiotic pea aphids Acyrthosiphon pisum. J Insect Physiol 36:35–40

    CAS  Google Scholar 

  • Sato S, Ishikawa H (1997a) Expression and control of an operon from an intracellular symbiont which is homologous to the groE operon. J Bacteriol 179:2300–2304

    CAS  PubMed  Google Scholar 

  • Sato S, Ishikawa H (1997b) Structure and expression of the dnaKJ operon of Buchnera, an intracellular symbiotic bacteria of aphid. J Biochem 122:41–48

    CAS  PubMed  Google Scholar 

  • Schröder D, Deppisch H, Obermayer M, Krohne G, Stackebrandt E, Holldobler B, Goebel W, Gross R (1996) Intracellular endosymbiotic bacteria of Camponotus species (carpenter ants): systematics, evolution and ultrastructural characterization. Mol Microbiol 21:479–489

    PubMed  Google Scholar 

  • Silva FJ, van Ham RCHJ, Sabater B, Latorre A (1998) Structure and evolution of the leucine plasmids carried by the endosymbiont (Buchnera aphidicola) from aphids of the family Aphididae. FEMS Microbiol Lett 168:43–49

    CAS  PubMed  Google Scholar 

  • Smith DC, Douglas AE (1987) The biology of symbiosis. Edward Arnold, London

    Google Scholar 

  • Smith OH, Yanofsky C (1962) Enzymes involved in the biosynthesis of tryptophan. Methods Enzymol 5:794–806

    CAS  Google Scholar 

  • Spaulding AW, von Dohlen CD (1998) Phylogenetic characterization and molecular evolution of bacterial endosymbionts in psyllids (Hemiptera: Sternorrhyncha). Mol Biol Evol 15:1506–1513

    CAS  PubMed  Google Scholar 

  • Stephens RS, Kalman S, Lammel C, Fan J, Marathe R, Aravind L, Mitchell W, Olinger L, Tatusov RL, Zhao QX, Koonin EV, Davis RW (1998) Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282:754–759

    CAS  PubMed  Google Scholar 

  • Sylvester ES (1985) Multiple acquisition of viruses and vector-dependent prokaryotes: consequences on transmission. Annu Rev Entomol 30:71–88

    Google Scholar 

  • Telang A, Sandström J, Dyreson E, Moran NA (1999) Feeding damage by Diuraphis noxia results in nutritionally enhanced phloem diet. Entomol Exp Appl 91:403–412

    Google Scholar 

  • Thao ML, Baumann P (1998) Sequence analysis of a DNA fragment from Buchnera aphidicola (aphid endosymbiont) containing the genes dapD-htrA-ilvI-ilvH-ftsL-ftsI-murE. Curr Microbiol 37:214–216

    CAS  PubMed  Google Scholar 

  • Thao ML, Baumann L, Baumann P, Moran NA (1998) Endosymbionts (Buchnera) from the aphids Schizaphis graminum and Diuraphis noxia have different copy numbers of the plasmid containing the leucine biosynthetic genes. Curr Microbiol 36:238–240

    CAS  PubMed  Google Scholar 

  • Tremblay E (1989) Coccoidea endosymbiosis. In: Schwemmler W, Gassner G (eds) Insect endocytobiosis: morphology, physiology, genetics, evolution. CRC Press, Boca Raton, pp 145–173

    Google Scholar 

  • Unterman BM, Baumann P (1990) Partial characterization of ribosomal RNA operons of the pea-aphid endosymbionts: evolutionary and physiological implications. In: Campbell RK, Eikenbary RD (eds) Aphid-plant genotype interactions. Elsevier Biomedical Press, Amsterdam, pp 329–350

    Google Scholar 

  • Unterman BM, Baumann P, McLean DL (1989) Pea aphid symbiont relationships established by analysis of 16S rRNAs. J Bacteriol 171:2970–2974

    CAS  PubMed  Google Scholar 

  • van den Heuvel JFJM, Verbeek M, van der Wilk F (1994) Endosymbiotic bacteria associated with circulative transmission of potato leafroll virus by Myzus persicae. J Gen Virol 75:2559–2565

    PubMed  Google Scholar 

  • van den Heuvel JFJM, Bruyere A, Hogenhout A, ZieglerGraff V, Brault V, Verbeek M, van derWilk F, Richards K (1997) The N-terminal region of the luteovirus readthrough domain determines virus binding to Buchnera GroEL and is essential for virus persistence in the aphid. J Virol 71:7258–7265

    PubMed  Google Scholar 

  • van Ham RCHJ, Moya A, Latorre A (1997) Putative evolutionary origin of plasmids carrying the genes involved in leucine biosynthesis in Buchnera aphidicola (endosymbiont of aphids). J Bacteriol 179:4768–4777

    PubMed  Google Scholar 

  • van Ham RCHJ, Martínez-Torres D, Moya A, Latorre A (1999) Plasmid-encoded anthranilate synthase (TrpEG) in Buchnera aphidicola from the family Pemphigidae. Appl Environ Microbiol 65:117–125

    Google Scholar 

  • von Dohlen CD, Moran NA (1995) Molecular phylogeny of the Homoptera—a paraphyletic taxon. J Mol Evol 41:211–223

    Google Scholar 

  • von Wintzingerode F, Gobel UB, Stackebrandt E (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21:213–229

    Google Scholar 

  • Waku Y, Endo Y (1987) Ultrastructure and life cycle of the symbionts in a Homopteran insect, Anomoneura mori Schwartz (Psyllidae). Appl Entomol Zool 22:630–637

    Google Scholar 

  • Wernegreen JJ, Moran NA (1999) Evidence for genetic drift in endosymbionts (Buchnera): analyses of protein-coding genes. Mol Biol Evol 16:83–97

    CAS  PubMed  Google Scholar 

  • Werren JH, O’Neill SL (1997) The evolution of heritable symbionts. In: O’Neill SL, Hoffman AA, Werren JH (eds) Influential passengers; inherited microorganisms and arthropod reproduction. Oxford University Press, Oxford, pp 1–41

    Google Scholar 

  • Whitehead LF, Douglas AE (1993) A metabolic study of Buchnera, the intracellular bacterial symbionts of the pea aphid Acyrthosiphon pisum. J Gen Microbiol 139:821–826

    CAS  Google Scholar 

  • Wicker C, Nardon P (1982) Development responses of symbiotic and aposymbiotic weevils Sitophilus oryzae L. (Coleoptera, Curculionidae) to a diet supplemented with aromatic amino-acids. J Insect Physiol 28:1021–1024

    CAS  Google Scholar 

  • Wilkinson TL (1998) The elimination of intracellular microorganisms from insects: an analysis of antibiotic-treatment in the pea aphid (Acyrthosiphon pisum). Comp Biochem Physiol A Comp Physiol 119:871–881

    Google Scholar 

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Authors and Affiliations

  1. Division of Agriculture and Natural Resources, University of California Cooperative Extension, Davis, CA, 95616-5224, USA

    Paul Baumann

  2. Biological and Biomedical Sciences Program, Yale University, New Haven, CT, USA

    Nancy A. Moran

  3. School of Nursing, University of Wisconsin-Madison, Madison, WI, 53792-2455, USA

    Linda C. Baumann

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  1. Paul Baumann
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  2. Nancy A. Moran
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  3. Linda C. Baumann
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Editors and Affiliations

  1. Department of Molecular Microbiology and Biotechnology, Tel Aviv University, Tel Aviv, Israel

    Eugene Rosenberg

  2. Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA

    Edward F. DeLong

  3. Department of Microbiology and Immunology, Harvard Medical School, Boston, MA, USA

    Stephen Lory

  4. Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany

    Erko Stackebrandt

  5. Laboratory of Microbiology, Institute of Biology, Center for Health Sciences, Federal University of Rio de Janeiro (UFRJ), Ilha do Fundão, Rio de Janeiro, Brazil

    Fabiano Thompson

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Baumann, P., Moran, N.A., Baumann, L.C. (2013). Bacteriocyte-Associated Endosymbionts of Insects. In: Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., Thompson, F. (eds) The Prokaryotes. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-30194-0_19

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