’ is an intracellularly multiplying bacterial pathogen of European cockchafers, (Linnaeus, 1758) and (Fabricius, 1801) (Coleoptera: Scarabaeidae). We report the first determination of nucleotide sequences from this organism, i.e. the 16S rRNA encoding gene, the chaperonin encoding gene and the gene encoding the orthologue of a capsule synthesis-inducing factor of . Within the genus , the pathotype ‘’ is currently classified as a synonym of the nomenclatural type species . Previous sequencing of a 16S rRNA gene from a different species, has motivated the transfer of the entire genus from the alphaproteobacterial order to the gammaproteobacterial order , family . We investigated the validity of this taxonomic reorganization beyond the species by reconstructing the organismal phylogeny from comparisons of 16S rRNA gene and GroEL and MucZ protein sequences from a selected set of alpha- and gammaproteobacteria as well as bacterial pathogens from the order . Our analysis strongly supported the transfer of the genus to the order , but not its classification in one of the recognized families present in this order. Furthermore, our results substantiated inconsistencies in the internal organization of the genus. In particular, the currently accepted delineation of species and the claimed synonymy of ‘’ with are not simultaneously consistent with our findings.


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  1. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J.(1997). Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25, 3389–3402.[CrossRef] [Google Scholar]
  2. Casiraghi, M., Bordenstein, S. R., Baldo, L., Lo, N., Beninati, T., Wernegreen, J. J., Werren, J. H. & Bandi, C.(2005). Phylogeny of Wolbachia pipientis based on gltA, groEL and ftsZ gene sequences: clustering of arthropod and nematode symbionts in the F supergroup, and evidence for further diversity in the Wolbachia tree. Microbiology 151, 4015–4022.[CrossRef] [Google Scholar]
  3. Cordaux, R., Paces-Fessy, M., Raimond, M., Michel-Salzat, A., Zimmer, M. & Bouchon, D.(2007). Molecular characterization and evolution of arthropod pathogenic Rickettsiella bacteria. Appl Environ Microbiol 73, 5045–5047.[CrossRef] [Google Scholar]
  4. Corsaro, D., Thomas, V., Goy, G., Venditti, D., Radek, R. & Greub, G.(2006).Candidatus Rhabdochlamydia crassificans’, an intracellular bacterial pathogen of the cockroach Blatta orientalis (Insecta: Blattodea). Syst Appl Microbiol 30, 221–228. [Google Scholar]
  5. Drobne, D., Strus, J., Znidarsic, N. & Zidar, P.(1999). Morphological description of bacterial infection of digestive glands in the terrestrial isopod Porcellio scaber (Isopoda, Crustacea). J Invertebr Pathol 73, 113–119.[CrossRef] [Google Scholar]
  6. Dutky, S. R. & Gooden, E. L.(1952).Coxiella popilliae, n. sp., a rickettsia causing blue disease of Japanese beetle larvae. J Bacteriol 63, 743–750. [Google Scholar]
  7. Everett, K. D. E., Bush, R. M. & Andersen, A. A.(1999). Emended description of the order Chlamydiales, proposal of Parachlamydiaceae fam. nov. and Simkaniaceae fam. nov., each containing one monotypic genus, revised taxonomy of the family Chlamydiaceae, including a new genus and five new species, and standards for the identification of organisms. Int J Syst Bacteriol 49, 415–440.[CrossRef] [Google Scholar]
  8. Fares, M. A., Moya, A. & Barrio, E.(2004). GroEL and the maintenance of bacterial endosymbiosis. Trends Genet 20, 413–416.[CrossRef] [Google Scholar]
  9. Federici, B. A.(1980). Reproduction and morphogenesis of Rickettsiella chironomi, an unusual intracellular procaryotic parasite of midge larvae. J Bacteriol 143, 995–1002. [Google Scholar]
  10. Fournier, P.-E. & Raoult, D.(2005). Genus II. Rickettsiella Philip 1956, 267AL. In Bergey's Manual of Systematic Bacteriology, pp. 241–247. Edited by G. M. Garrity, D. J. Brenner, N. R. Krieg & J. T. Staley. New York: Springer.
  11. Frutos, R., Federici, B. A., Revet, B. & Bergoin, M.(1994). Taxonomic studies of Rickettsiella, Rickettsia, and Chlamydia using genomic DNA. J Invertebr Pathol 63, 294–300.[CrossRef] [Google Scholar]
  12. Garduño, R. A., Garduño, E. & Hoffman, P. S.(1998). Surface-associated Hsp60 chaperonin of Legionella pneumophila mediates invasion in a HeLa cell model. Infect Immun 66, 4602–4610. [Google Scholar]
  13. Garrity, G. M., Bell, J. A. & Lilburn, T.(2005). Family II. Coxiellaceae fam. nov. In Bergey's Manual of Systematic Bacteriology, pp. 237–247. Edited by G. M. Garrity, D. J. Brenner, N. R. Krieg & J. T. Staley. New York: Springer.
  14. Götz, P.(1972).Rickettsiella chironomi’: An unusual bacterial pathogen which reproduces by multiple cell division. J Invertebr Pathol 20, 22–30.[CrossRef] [Google Scholar]
  15. Guindon, S. & Gascuel, O.(2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52, 696–704.[CrossRef] [Google Scholar]
  16. Hasegawa, M., Kishino, H. & Yano, T.-A.(1985). Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22, 160–174.[CrossRef] [Google Scholar]
  17. Hall, I. M. & Badgley, M. E.(1957). A Rickettsial disease of larvae of species of Stethorus caused by Rickettsiella stethorae, n. sp. J Bacteriol 74, 452–455. [Google Scholar]
  18. Huger, A. M.(1963). Eine Rickettsiose der Orientalischen Schabe, Blatta orientalis L., verursacht durch Rickettsiella blattae nov. spec. Naturwissenschaften 51, 22(in German). [Google Scholar]
  19. Huger, A. M. & Krieg, A.(1967). New aspects of the mode of reproduction of Rickettsiella organisms in insects. J Invertebr Pathol 9, 442–445.[CrossRef] [Google Scholar]
  20. Jones, D. T., Taylor, W. R. & Thornton, J. M.(1992). The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8, 275–282. [Google Scholar]
  21. Kimura, M.(1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16, 111–120.[CrossRef] [Google Scholar]
  22. Kostanjsek, R., Strus, J., Drobne, D. & Avgustin, G.(2004). ‘Candidatus Rhabdochlamydia porcellionis’, an intracellular bacterium from the hepatopancreas of the terrestrial isopod Porcellio scaber (Crustacea: Isopoda). Int J Syst Evol Microbiol 54, 543–549.[CrossRef] [Google Scholar]
  23. Krieg, A.(1955). Licht- und elektronenmikroskopische Untersuchungen zur Pathologie der ‘Lorscher Erkrankung’ von Engerlingen und zur Zytologie der Rickettsia melolonthae nov. spec. Z Naturforsch B 10b, 34–37 (in German). [Google Scholar]
  24. Krieg, A.(1958a). Weitere Untersuchungen zur Pathologie der Rickettsiose von Melolontha spec. Z Naturforsch B 13b, 374–379 (in German). [Google Scholar]
  25. Krieg, A.(1958b). Vergleichende taxonomische, morphologische und serologische Untersuchungen an insektenpathogenen Rickettsien. Z Naturforsch B 13b, 555–557 (in German). [Google Scholar]
  26. Krieg, A.(1960). Elektronenmikroskopische Untersuchungen zur Rickettsiose von Melolontha melolontha (L.) an Hand von Ultra-Dünnschnitten. Z Naturforsch B 15b, 31–33 (in German). [Google Scholar]
  27. Kumar, S., Tamura, K. & Nei, M.(2004).mega3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5, 150–163.[CrossRef] [Google Scholar]
  28. Kurtti, T. J., Palmer, A. T. & Oliver, J. H.(2002).Rickettsiella-like bacteria in Ixodes woodi (Acari: Ixodidae). J Med Entomol 39, 534–540.[CrossRef] [Google Scholar]
  29. McNally, D. & Fares, M. A.(2007).In silico identification of functional divergence between the multiple groEL gene paralogs in Chlamydiae. BMC Evol Biol 7, 81[CrossRef] [Google Scholar]
  30. Philip, C. B.(1956). Comments on the classification of the order Rickettsiales. Can J Microbiol 2, 261–270.[CrossRef] [Google Scholar]
  31. Posada, D. & Crandall, K. A.(1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.[CrossRef] [Google Scholar]
  32. Radek, R.(2000). Light and electron microscopic study of a Rickettsiella species from the cockroach Blatta orientalis. J Invertebr Pathol 76, 249–256.[CrossRef] [Google Scholar]
  33. Roux, V., Bergoin, M., Lamaze, N. & Raoult, D.(1997). Reassessment of the taxonomic position of Rickettsiella grylli. Int J Syst Bacteriol 47, 1255–1257.[CrossRef] [Google Scholar]
  34. Schmidt, H. A., Strimmer, K., Vingron, M. & von Haeseler, A.(2002).tree-puzzle: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18, 502–504.[CrossRef] [Google Scholar]
  35. Sekeyová, Z., Roux, V. & Raoult, D.(1999). Intraspecies diversity of Coxiella burnetii as revealed by com1 and mucZ sequence comparison. FEMS Microbiol Lett 180, 61–67.[CrossRef] [Google Scholar]
  36. Stein, A., Saunders, N. A., Taylor, A. G. & Raoult, D.(1993). Phylogenetic homogeneity of Coxiella burnetii strains as determined by 16S ribosomal RNA sequencing. FEMS Microbiol Lett 113, 339–344.[CrossRef] [Google Scholar]
  37. Tanada, Y. & Kaya, H. K.(1993).Insect Pathology, pp. 153–158. San Diego, CA: Academic Press.
  38. Thompson, J. D., Higgins, D. G. & Gibson, T. J.(1994).clustalw: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680.[CrossRef] [Google Scholar]
  39. Vago, C. & Martoja, R.(1963). Une rickettsiose chez les Gryllidae (Orthoptera). C R Hebd Seances Acad Sci 256, 1045–1047 (in French). [Google Scholar]
  40. Viale, A. M., Arakaki, A. K., Soncini, F. C. & Ferreyra, R. G.(1994). Evolutionary relationships among eubacterial groups as inferred from GroEL (chaperonin) sequence comparisons. Int J Syst Bacteriol 44, 527–533.[CrossRef] [Google Scholar]
  41. Walsh, P. S., Metzger, D. A. & Higuchi, R.(1991). Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10, 506–513. [Google Scholar]
  42. Weisburg, W. G., Dobson, M. E., Samuel, J. E., Dasch, G. A., Mallavia, L. P., Baca, O., Mandelco, L., Sechrest, J. E., Weiss, E. & Woese, C. R.(1989). Phylogenetic diversity of the rickettsiae. J Bacteriol 171, 4202–4206. [Google Scholar]
  43. 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]
  44. Weiser, J.(1963). Diseases of insects of medical importance in Europe. Bull World Health Organ 28, 121–127. [Google Scholar]
  45. Weiss, E. & Moulder, J. W.(1984). Order I. Rickettsiales Gieszczkiewicz 1939. In Bergey's Manual of Systematic Bacteriology, pp. 687–729. Edited by N. R. Krieg & J. G. Holt. Baltimore, MD: Williams & Wilkins.
  46. Wille, H. & Martignoni, M. E.(1952). Vorläufige Mitteilung über einen neuen Krankheitstypus beim Engerling von Melolontha vulgaris F. Schweiz Z Pathol Bakteriol 15, 470–473 (in German). [Google Scholar]
  47. Yang, Z.(1993). Maximum-likelihood estimation of phylogeny from DNA sequences when substitution rates differ over sites. Mol Biol Evol 10, 1396–1401. [Google Scholar]
  48. Zuber, M., Hoover, T. A. & Court, D. L.(1995). Analysis of a Coxiella burnetii gene product that activates capsule synthesis in Escherichia coli: requirement for the heat shock chaperone DnaK and the two-component regulator RcsC. J Bacteriol 177, 4238–4244. [Google Scholar]

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