1887

Abstract

Symbiotic interactions with bacteria are essential for the survival and reproduction of many insects. The European beewolf (, Hymenoptera, Crabronidae) engages in a highly specific association with bacteria of the genus that appears to protect beewolf offspring against infection by pathogens. Using transmission and scanning electron microscopy, the bacteria were located in the antennal glands of female wasps, where they form dense cell clusters. Using genetic methods, closely related streptomycetes were found in the antennae of 27 species (including two subspecies of from distant localities). In contrast, no endosymbionts could be detected in the antennae of other genera within the subfamily Philanthinae (, and ). On the basis of morphological, genetic and ecological data, ‘ Streptomyces philanthi’ is proposed. 16S rRNA gene sequence data are provided for 28 ecotypes of ‘ Streptomyces philanthi’ that reside in different host species and subspecies of the genus . Primers for the selective amplification of ‘ Streptomyces philanthi’ and an oligonucleotide probe for specific detection by fluorescence hybridization (FISH) are described.

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2006-06-01
2019-10-14
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References

  1. 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.[CrossRef]
    [Google Scholar]
  2. Amann, R. I., Binder, B. J., Olson, R. J., Chisholm, S. W., Devereux, R. & Stahl, D. A. ( 1990; ). Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56, 1919–1925.
    [Google Scholar]
  3. Bandi, C., Damiani, G., Magrassi, L., Grigolo, A., Fani, R. & Sacchi, L. ( 1994; ). Flavobacteria as intracellular symbionts in cockroaches. Proc Biol Sci 257, 43–48.[CrossRef]
    [Google Scholar]
  4. Bandi, C., Sironi, M., Damiani, G., Magrassi, L., Nalepa, C. A., Laudani, U. & Sacchi, L. ( 1995; ). The establishment of intracellular symbiosis in an ancestor of cockroaches and termites. Proc Biol Sci 259, 293–299.[CrossRef]
    [Google Scholar]
  5. Baumann, P. & Moran, N. A. ( 1997; ). Non-cultivable microorganisms from symbiotic associations of insects and other hosts. Antonie van Leeuwenhoek 72, 39–48.[CrossRef]
    [Google Scholar]
  6. Baumann, P., Moran, N. A. & Baumann, L. ( 1997; ). The evolution and genetics of aphid endosymbionts. Bioscience 47, 12–20.[CrossRef]
    [Google Scholar]
  7. Bohart, R. M. & Grissell, E. E. ( 1975; ). California wasps of the subfamily Philanthinae (Hymenoptera: Sphecidae). Bull Calif Insect Surv 19, 1–57.
    [Google Scholar]
  8. Bourtzis, K. & Miller, T. A. (editors) ( 2003; ). Insect Symbiosis. Boca Raton, FL: CRC Press.
  9. Buchner, P. ( 1921; ). Tier und Pflanze in Intrazellulärer Symbiose. Berlin: Verlag Gebrüder Borntraeger (in German).
  10. Cafaro, M. J. & Currie, C. R. ( 2005; ). Phylogenetic analysis of mutualistic filamentous bacteria associated with fungus-growing ants. Can J Microbiol 51, 441–446.[CrossRef]
    [Google Scholar]
  11. Chen, X. O., Li, C. B., Zhao, S. Y. & Aksoy, S. ( 1999; ). Phylogeny of the symbionts of tsetse and the evolutionary relationships with their hosts. Prog Nat Sci 9, 922–928.
    [Google Scholar]
  12. Clark, M. A., Moran, N. A., Baumann, P. & Wernegreen, J. J. ( 2000; ). Cospeciation between bacterial endosymbionts (Buchnera) and a recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution Int J Org Evolution 54, 517–525.[CrossRef]
    [Google Scholar]
  13. Clark, J. W., Hossain, S., Burnside, C. A. & Kambhampati, S. ( 2001; ). Coevolution between a cockroach and its bacterial endosymbiont: a biogeographical perspective. Proc Biol Sci 268, 393–398.[CrossRef]
    [Google Scholar]
  14. Cohan, F. M. ( 2002; ). What are bacterial species? Annu Rev Microbiol 56, 457–487.[CrossRef]
    [Google Scholar]
  15. Currie, C. R., Scott, J. A., Summerbell, R. C. & Malloch, D. ( 1999; ). Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398, 701–704.[CrossRef]
    [Google Scholar]
  16. Douglas, A. E. ( 1998; ). Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43, 17–37.[CrossRef]
    [Google Scholar]
  17. Ferguson, G. R. ( 1983a; ). Two new species in the genus Philanthus and a key to the politus group (Hymenoptera, Philanthidae). Pan-Pacific Entomol 59, 55–63.
    [Google Scholar]
  18. Ferguson, G. R. ( 1983b; ). Revision of the Philanthus zebratus group (Hymenoptera, Philanthidae). J N Y Entomol Soc 91, 289–303.
    [Google Scholar]
  19. Grimm, D., Merkert, H., Ludwig, W., Schleifer, K. H., Hacker, J. & Brand, B. C. ( 1998; ). Specific detection of Legionella pneumophila: construction of a new 16S rRNA-targeted oligonucleotide probe. Appl Environ Microbiol 64, 2686–2690.
    [Google Scholar]
  20. Ishikawa, H. ( 2003; ). Insect symbiosis: an introduction. In Insect Symbiosis, pp. 1–21. Edited by K. Bourtzis & T. A. Miller. Boca Raton, FL: CRC Press.
  21. Kaltenpoth, M., Göttler, W., Herzner, G. & Strohm, E. ( 2005; ). Symbiotic bacteria protect wasp larvae from fungal infestation. Curr Biol 15, 475–479.[CrossRef]
    [Google Scholar]
  22. Konstantinidis, K. T. & Tiedje, J. M. ( 2005; ). Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci U S A 102, 2567–2572.[CrossRef]
    [Google Scholar]
  23. Liu, Z. H., Shi, Y. L., Zhang, Y. M., Zhou, Z. H., Lu, Z. T., Li, W., Huang, Y., Rodriguez, C. & Goodfellow, M. ( 2005; ). Classification of Streptomyces griseus (Krainsky 1914) Waksman and Henrici 1948 and related species and the transfer of ‘Microstreptospora cinerea’ to the genus Streptomyces as Streptomyces yanii sp. nov. Int J Syst Evol Microbiol 55, 1605–1610.[CrossRef]
    [Google Scholar]
  24. Lo, N., Bandi, C., Watanabe, H., Nalepa, C. & Beninati, T. ( 2003; ). Evidence for cocladogenesis between diverse dictyopteran lineages and their intracellular endosymbionts. Mol Biol Evol 20, 907–913.[CrossRef]
    [Google Scholar]
  25. Manfio, G. P., Atalan, E., Zakrzewska-Czerwinska, J., Mordarski, M., Rodriguez, C., Collins, M. D. & Goodfellow, M. ( 2003; ). Classification of novel soil streptomycetes as Streptomyces aureus sp. nov., Streptomyces laceyi sp. nov. and Streptomyces sanglieri sp. nov. Antonie van Leeuwenhoek 83, 245–255.[CrossRef]
    [Google Scholar]
  26. McFall-Ngai, M. J. & Ruby, E. G. ( 1991; ). Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterial mutualism. Science 254, 1491–1493.[CrossRef]
    [Google Scholar]
  27. Moran, N. & Baumann, P. ( 1994; ). Phylogenetics of cytoplasmically inherited microorganisms of arthropods. Trends Ecol Evol 9, 15–20.[CrossRef]
    [Google Scholar]
  28. Moran, N. A. & Baumann, P. ( 2000; ). Bacterial endosymbionts in animals. Curr Opin Microbiol 3, 270–275.[CrossRef]
    [Google Scholar]
  29. Moran, N. A. & Telang, A. ( 1998; ). Bacteriocyte-associated symbionts of insects. Bioscience 48, 295–304.[CrossRef]
    [Google Scholar]
  30. Moran, N. A., Munson, M. A., Baumann, P. & Ishikawa, H. ( 1993; ). A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc Biol Sci 253, 167–171.[CrossRef]
    [Google Scholar]
  31. Nishiguchi, M. K. ( 2002; ). Host-symbiont recognition in the environmentally transmitted sepiolid squid-Vibrio mutualism. Microb Ecol 44, 10–18.[CrossRef]
    [Google Scholar]
  32. Nyholm, S. V. & McFall-Ngai, M. J. ( 2004; ). The winnowing: establishing the squid-Vibrio symbiosis. Nat Rev Microbiol 2, 632–642.[CrossRef]
    [Google Scholar]
  33. Nyholm, S. V., Stabb, E. V., Ruby, E. G. & McFall-Ngai, M. J. ( 2000; ). Establishment of an animal-bacterial association: recruiting symbiotic vibrios from the environment. Proc Natl Acad Sci U S A 97, 10231–10235.[CrossRef]
    [Google Scholar]
  34. Ochman, H. & Wilson, A. C. ( 1987; ). Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 26, 74–86.[CrossRef]
    [Google Scholar]
  35. Pernodet, J. L., Boccard, F., Alegre, M. T., Gagnat, J. & Guerineau, M. ( 1989; ). Organization and nucleotide sequence analysis of a ribosomal RNA gene cluster from Streptomyces ambofaciens. Gene 79, 33–46.[CrossRef]
    [Google Scholar]
  36. Priest, F. G. & Dewar, S. J. ( 2000; ). Bacteria and insects. In Applied Microbial Systematics, pp. 165–202. Edited by F. G. Priest & M. Goodfellow. Dordrecht: Kluwer Academic.
  37. Rintala, H., Nevalainen, A., Ronka, E. & Suutari, M. ( 2001; ). PCR primers targeting the 16S rRNA gene for the specific detection of streptomycetes. Mol Cell Probes 15, 337–347.[CrossRef]
    [Google Scholar]
  38. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  39. Sauer, C., Stackebrandt, E., Gadau, J., Holldobler, B. & Gross, R. ( 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, 1877–1886.
    [Google Scholar]
  40. Sauer, C., Dudaczek, D., Holldobler, B. & Gross, R. ( 2002; ). Tissue localization of the endosymbiotic bacterium ‘Candidatus Blochmannia floridanus' in adults and larvae of the carpenter ant Camponotus floridanus. Appl Environ Microbiol 68, 4187–4193.[CrossRef]
    [Google Scholar]
  41. Sembiring, L., Ward, A. C. & Goodfellow, M. ( 2000; ). Selective isolation and characterisation of members of the Streptomyces violaceusniger clade associated with the roots of Paraserianthes falcataria. Antonie van Leeuwenhoek 78, 353–366.[CrossRef]
    [Google Scholar]
  42. Stach, J. E. M., Maldonado, L. A., Ward, A. C., Goodfellow, M. & Bull, A. T. ( 2003; ). New primers for the class Actinobacteria: application to marine and terrestrial environments. Environ Microbiol 5, 828–841.[CrossRef]
    [Google Scholar]
  43. Strohm, E. ( 1995; ). Allokation elterlicher Investitionen beim Europäischen Bienenwolf Philanthus triangulum Fabricius (Hymenoptera: Sphecidae). Berlin: Verlag Dr. Köster (in German).
  44. Strohm, E. & Linsenmair, K. E. ( 1995; ). Leaving the cradle: how beewolves (Philanthus triangulum F.) obtain the necessary spatial information for emergence. Zoology (Jena) 98, 137–146.
    [Google Scholar]
  45. Strohm, E. & Linsenmair, K. E. ( 2001; ). Females of the European beewolf preserve their honeybee prey against competing fungi. Ecol Entomol 26, 198–203.[CrossRef]
    [Google Scholar]
  46. Weisburg, W. G., Barns, S. M., Pelletier, D. A. & Lane, D. J. ( 1991; ). 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173, 697–703.
    [Google Scholar]
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vol. , part 6, pp. 1403 - 1411

A description of the methods used in attempts to cultivate ‘ Streptomyces philanthi’. [PDF](61 KB)



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