1887

Abstract

Chlamydiae are a unique group of obligate intracellular bacteria comprising important pathogens of vertebrates as well as symbionts of free-living amoebae. Although there is ample molecular evidence for a huge diversity and wide distribution of chlamydiae in nature, environmental chlamydiae are currently represented by only few isolates. This paper reports the recovery of a novel environmental chlamydia strain from activated sludge by co-cultivation with sp. The recovered environmental chlamydia strain UV-7 showed the characteristic morphology of chlamydial developmental stages as revealed by electron microscopy and was identified as a new member of the family (98·7 % 16S rRNA sequence similarity to ). Infection studies suggested that sp. UV-7 is not confined to amoeba hosts but is also able to invade mammalian cells. These findings outline a new straightforward approach to retrieving environmental chlamydiae from nature without prior, tedious isolation and cultivation of their natural host cells, and lend further support to suggested implications of environmental chlamydiae for public health.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27406-0
2005-01-01
2019-10-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/1/mic1510301.html?itemId=/content/journal/micro/10.1099/mic.0.27406-0&mimeType=html&fmt=ahah

References

  1. Abd, H., Johansson, T., Golovliov, I., Sandstrom, G. & Forsman, M. ( 2003; ). Survival and growth of Francisella tularensis in Acanthamoeba castellanii. Appl Environ Microbiol 69, 600–606.[CrossRef]
    [Google Scholar]
  2. Alm, E. W., Oerther, D. B., Larsen, N., Stahl, D. A. & Raskin, L. ( 1996; ). The oligonucleotide probe database. App Environ Microbiol 62, 3557–3559.
    [Google Scholar]
  3. Amann, R., 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]
  4. Amann, R., Springer, N., Schönhuber, W., Ludwig, W., Schmid, E. N., Müller, K. D. & Michel, R. ( 1997; ). Obligate intracellular bacterial parasites of acanthamoebae related to Chlamydia spp. Appl Environ Microbiol 63, 115–121.
    [Google Scholar]
  5. Barker, J., Humphrey, T. J. & Brown, M. W. R. ( 1999; ). Survival of Escherichia coli O157 in a soil protozoan: implications for disease. FEMS Microbiol Lett 173, 291–295.[CrossRef]
    [Google Scholar]
  6. Beier, C. L., Horn, M., Michel, R., Schweikert, M., Görtz, H. D. & Wagner, M. ( 2002; ). The genus Caedibacter comprises endosymbionts of Paramecium spp. related to the Rickettsiales (Alphaproteobacteria) and to Francisella tularensis (Gammaproteobacteria). Appl Environ Microbiol 68, 6043–6050.[CrossRef]
    [Google Scholar]
  7. Birtles, R. J., Rowbotham, T. J., Storey, C., Marrie, T. J. & Raoult, D. ( 1997; ). Chlamydia-like obligate parasite of free-living amoebae. Lancet 349, 925–926.[CrossRef]
    [Google Scholar]
  8. Birtles, R. J., Rowbotham, T. J., Michel, R., Pitcher, D. G., Lascola, B., Alexiou-Daniel, S. & Raoult, D. ( 2000; ).Candidatus Odyssella thessalonicensis' gen. nov., sp. nov., an obligate intracellular parasite of Acanthamoeba species. Int J Syst Evol Microbiol 50, 63–72.[CrossRef]
    [Google Scholar]
  9. Bodetti, T. J., Viggers, K., Warren, K., Swan, R., Conaghty, S., Sims, C. & Timms, P. ( 2003; ). Wide range of Chlamydiales types detected in native Australian mammals. Vet Microbiol 96, 177–187.[CrossRef]
    [Google Scholar]
  10. Corsaro, D., Venditti, D., Le Faou, A., Guglielmetti, P. & Valassina, M. ( 2001; ). A new chlamydia-like 16S rDNA sequence from a clinical sample. Microbiology 147, 515–516.
    [Google Scholar]
  11. Corsaro, D., Venditti, D. & Valassina, M. ( 2002a; ). New parachlamydial 16S rDNA phylotypes detected in human clinical samples. Res Microbiol 153, 563–567.[CrossRef]
    [Google Scholar]
  12. Corsaro, D., Venditti, D. & Valassina, M. ( 2002b; ). New chlamydial lineages from freshwater samples. Microbiology 148, 343–344.
    [Google Scholar]
  13. Corsaro, D., Valassina, M. & Venditti, D. ( 2003; ). Increasing diversity within chlamydiae. Crit Rev Microbiol 29, 37–78.[CrossRef]
    [Google Scholar]
  14. Daims, H., Brühl, A., Amann, R., Schleifer, K.-H. & Wagner, M. ( 1999; ). The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22, 434–444.[CrossRef]
    [Google Scholar]
  15. Daims, H., Stoecker, K. & Wagner, M. ( 2005; ). Fluorescence in situ hybridisation for the detection of prokaryotes. In Molecular Microbial Ecology. Edited by A. M. Osborn & C. J. Smith. Abingdon, UK: Bios-Garland (in press).
  16. Dowell, S. F., Peeling, R. W., Boman, J. & 12 other authors ( 2001; ). Standardizing Chlamydia pneumoniae assays: recommendations from the Centers for Disease Control and Prevention (USA) and the Laboratory Centre for Disease Control (Canada). Clin Infect Dis 33, 492–503.[CrossRef]
    [Google Scholar]
  17. Essig, A., Heinemann, M., Simnacher, U. & Marre, R. ( 1997; ). Infection of Acanthamoeba castellanii by Chlamydia pneumoniae. Appl Environ Microbiol 63, 1396–1399.
    [Google Scholar]
  18. Everett, K. D., 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]
  19. Felsenstein, J. ( 1989; ). PHYLIP – phylogeny inference package (version 3.2). Cladistics 5, 164–166.
    [Google Scholar]
  20. Friedman, M. G., Dvoskin, B. & Kahane, S. ( 2003; ). Infections with the chlamydia-like microorganism Simkania negevensis, a possible emerging pathogen. Microbes Infect 5, 1013–1021.[CrossRef]
    [Google Scholar]
  21. Fritsche, T. R., Gautom, R. K., Seyedirashti, S., Bergeron, D. L. & Lindquist, T. D. ( 1993; ). Occurrence of bacteria endosymbionts in Acanthamoeba spp. isolated from corneal and environmental specimens and contact lenses. J Clin Microbiol 31, 1122–1126.
    [Google Scholar]
  22. Fritsche, T. R., Sobek, D. & Gautom, R. K. ( 1998; ). Enhancement of in vitro cytopathogenicity by Acanthamoeba spp. following acquisition of bacterial endosymbionts. FEMS Microbiol Lett 166, 231–236.[CrossRef]
    [Google Scholar]
  23. Fritsche, T. R., Horn, M., Seyedirashti, S., Gautom, R. K., Schleifer, K. H. & Wagner, M. ( 1999; ). In situ detection of novel bacterial endosymbionts of Acanthamoeba spp. phylogenetically related to members of the order Rickettsiales. Appl Environ Microbiol 65, 206–212.
    [Google Scholar]
  24. Fritsche, T. R., Horn, M., Wagner, M., Herwig, R. P., Schleifer, K. H. & Gautom, R. K. ( 2000; ). Phylogenetic diversity among geographically dispersed Chlamydiales endosymbionts recovered from clinical and environmental isolates of Acanthamoeba spp. Appl Environ Microbiol 66, 2613–2619.[CrossRef]
    [Google Scholar]
  25. Gautom, R. & Fritsche, T. R. ( 1995; ). Transmissibility of bacterial endosymbionts between isolates of Acanthamoeba spp. J Eukaryot Microbiol 42, 452–456.[CrossRef]
    [Google Scholar]
  26. Goebel, W. & Gross, R. ( 2001; ). Intracellular survival strategies of mutualistic and parasitic prokaryotes. Trends Microbiol 9, 267–273.[CrossRef]
    [Google Scholar]
  27. Greene, W., Xiao, Y., Huang, Y., McClarty, G. & Zhong, G. ( 2004; ). Chlamydia-infected cells continue to undergo mitosis and resist induction of apoptosis. Infect Immun 72, 451–460.[CrossRef]
    [Google Scholar]
  28. Greub, G. & Raoult, D. ( 2002a; ). Crescent bodies of Parachlamydia acanthamoeba and its life cycle within Acanthamoeba polyphaga: an electron micrograph study. Appl Environ Microbiol 68, 3076–3084.[CrossRef]
    [Google Scholar]
  29. Greub, G. & Raoult, D. ( 2002b; ). Parachlamydiaceae: potential emerging pathogens. Emerg Infect Dis 8, 625–630.
    [Google Scholar]
  30. Greub, G., Boyadjiev, I., La Scola, B., Raoult, D. & Martin, C. ( 2003a; ). Serological hint suggesting that Parachlamydiaceae are agents of pneumonia in polytraumatized intensive care patients. Ann N Y Acad Sci 990, 311–319.[CrossRef]
    [Google Scholar]
  31. Greub, G., Mege, J.-L. & Raoult, D. ( 2003b; ). Parachlamydia acanthamoeba enters and multiplies within human macrophages and induces their apoptosis. Infect Immun 71, 5979–5985.[CrossRef]
    [Google Scholar]
  32. Greub, G., La Scola, B. & Raoult, D. ( 2004; ). Amoebae-resisting bacteria isolated from human nasal swabs by amoebal co-culture. Emerg Infect Dis 10, 470–477.[CrossRef]
    [Google Scholar]
  33. Harb, O. S., Gao, L.-Y. & Kwaik, Y. A. ( 2000; ). From protozoa to mammalian cells: a new paradigm in the life cycle of intracellular bacterial pathogens. Environ Microbiol 2, 251–265.[CrossRef]
    [Google Scholar]
  34. Henning, K., Schares, G., Granzow, H., Polster, U., Hartmann, M., Hotzel, H., Sachse, K., Peters, M. & Rauser, M. ( 2002; ). Neospora caninum and Waddlia chondrophila strain 2032/99 in a septic stillborn calf. Vet Microbiol 85, 285–292.[CrossRef]
    [Google Scholar]
  35. Horn, M. & Wagner, M. ( 2001; ). Evidence for additional genus-level diversity of Chlamydiales in the environment. FEMS Microbiol Lett 204, 71–74.[CrossRef]
    [Google Scholar]
  36. Horn, M., Wagner, M., Müller, K. D., Schmid, E. N., Fritsche, T. R., Schleifer, K. H. & Michel, R. ( 2000; ). Neochlamydia hartmannellae gen. nov., sp. nov. (Parachlamydiaceae), an endoparasite of the amoeba Hartmannella vermiformis. Microbiology 146, 1231–1239.
    [Google Scholar]
  37. Horn, M., Harzenetter, M. D., Linner, T., Schmid, E. N., Müller, K. D., Michel, R. & Wagner, M. ( 2001; ). Members of the Cytophaga-Flavobacterium-Bacteroides phylum as intracellular bacteria of acanthamoebae: proposal of ‘Candidatus Amoebophilus asiaticus’. Environ Microbiol 3, 440–449.[CrossRef]
    [Google Scholar]
  38. Horn, M., Fritsche, T. R., Linner, T., Gautom, R. K., Harzenetter, M. D. & Wagner, M. ( 2002; ). Obligate bacterial endosymbionts of Acanthamoeba spp. related to the beta-Proteobacteria: proposal of ‘Candidatus Procabacter acanthamoebae’ gen. nov., sp. nov. Int J Syst Evol Microbiol 52, 599–605.
    [Google Scholar]
  39. Horn, M., Collingro, A., Schmitz-Esser, S. & 10 other authors ( 2004; ). Illuminating the evolutionary history of chlamydiae. Science 304, 728–730.[CrossRef]
    [Google Scholar]
  40. Kahane, S. E. M. & Friedman, M. G. ( 1995; ). Evidence that the novel microorganism ‘Z’ may belong to a new genus in the family Chlamydiaceae. FEMS Microbiol Lett 126, 203–208.[CrossRef]
    [Google Scholar]
  41. Kahane, S., Dvoskin, B., Mathias, M. & Friedman, M. G. ( 2001; ). Infection of Acanthamoeba polyphaga with Simkania negevensis and S. negevensis survival within amoebal cysts. Appl Environ Microbiol 67, 4789–4795.[CrossRef]
    [Google Scholar]
  42. Kahane, S., Kimmel, N. & Friedman, M. G. ( 2002; ). The growth cycle of Simkania negevensis. Microbiology 148, 735–742.
    [Google Scholar]
  43. Kahane, S., Platzner, N., Dvoskin, B., Itzhaki, A. & Friedman, M. G. ( 2004; ). Evidence for the presence of Simkania negevensis in drinking water and in reclaimed wastewater in Israel. Appl Environ Microbiol 70, 3346–3351.[CrossRef]
    [Google Scholar]
  44. 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]
  45. Lindsay, M. R., Webb, R. I., Hosmer, H. M. & Fuerst, J. A. ( 1995; ). Effects of fixative and buffer on morphology and ultrastructure of a freshwater planctomycete, Gemmata obscuriglobus. J Microbiol Methods 21, 45–54.[CrossRef]
    [Google Scholar]
  46. Loy, A., Horn, M. & Wagner, M. ( 2003; ). probeBase: an online resource for rRNA-targeted oligonucleotide probes. Nucleic Acids Res 31, 514–516.[CrossRef]
    [Google Scholar]
  47. Ludwig, W., Strunk, O., Westram, R. & 29 other authors ( 2004; ). ARB: a software environment for sequence data. Nucleic Acids Res 32, 1363–1371.[CrossRef]
    [Google Scholar]
  48. Mahoney, J. B., Coombes, B. K. & Chernesky, M. A. ( 2003; ). Chlamydia and Chlamydophila. In Manual of Clinical Microbiology, pp. 991–1004. Edited by P. R. Murray. Washington, DC: American Society for Microbiology.
  49. Marrie, T. J., Raoult, D., La Scola, B., Birtles, R. J. & de Carolis, E. ( 2001; ). Legionella-like and other amoebal pathogens as agents of community-acquired pneumonia. Emerg Infect Dis 7, 1026–1029.[CrossRef]
    [Google Scholar]
  50. Michel, R., Hauröder-Philippczyk, B., Müller, K.-D. & Weishaar, I. ( 1994; ). Acanthamoeba from human nasal mucosa infected with an obligate intracellular parasite. Eur J Protistol 30, 104.[CrossRef]
    [Google Scholar]
  51. Michel, R., Steinert, M., Zöller, L., Hauröder, B. & Henning, K. ( 2004; ). Free-living amoebae may serve as hosts for the chlamydia-like bacterium Waddlia chondrophila isolated from an aborted bovine foetus. Acta Protozool 43, 37–42.
    [Google Scholar]
  52. Neal, R. A., Latter, V. S. & Richards, W. H. ( 1974; ). Survival of Entamoeba and related amoebae at low temperature. II. Viability of amoebae and cysts stored in liquid nitrogen. Int J Parasitol 4, 353–360.[CrossRef]
    [Google Scholar]
  53. Ossewaarde, J. M. & Meijer, A. ( 1999; ). Molecular evidence for the existence of additional members of the order Chlamydiales. Microbiology 145, 411–417.[CrossRef]
    [Google Scholar]
  54. Page, F. C. ( 1988; ). A New Key to Freshwater and Soil Gymnamoebae. Ambleside, UK: Freshwater Biological Association.
  55. Pudjiatmoko, H. F., Ochiai, Y., Yamaguchi, T. & Hirai, K. ( 1997; ). Phylogenetic analysis of the genus Chlamydia based on 16S rRNA gene sequences. Int J Syst Bacteriol 45, 425–431.
    [Google Scholar]
  56. Rockey, D. D., Lenart, J. & Stephens, R. S. ( 2000; ). Genome sequencing and our understanding of chlamydiae. Infect Immun 68, 5473–5479.[CrossRef]
    [Google Scholar]
  57. Rowbotham, T. J. ( 1983; ). Isolation of Legionella pneumophila from clinical specimens via amoebae, and the interaction of those and other isolates with amoebae. J Clin Pathol 36, 978–986.[CrossRef]
    [Google Scholar]
  58. Rurangirwa, F. R., Dilbeck, P. M., Crawford, T. B., McGuire, T. C. & McElwain, T. F. ( 1999; ). Analysis of the 16S rRNA gene of microorganism WSU 86-1044 from an aborted bovine foetus reveals that it is a member of the order Chlamydiales: proposal of Waddliaceae fam. nov., Waddlia chondrophila gen. nov., sp. nov. Int J Syst Bacteriol 49, 577–581.[CrossRef]
    [Google Scholar]
  59. Schoier, J., Ollinger, K., Kvarnstrom, M., Soderlund, G. & Kihlstrom, E. ( 2001; ). Chlamydia trachomatis-induced apoptosis occurs in uninfected McCoy cells late in the developmental cycle and is regulated by the intracellular redox state. Microb Pathog 31, 173–184.[CrossRef]
    [Google Scholar]
  60. Stackebrandt, E. & Goebel, B. M. ( 1994; ). Taxonomic note: a place for DNA–DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44, 846–849.[CrossRef]
    [Google Scholar]
  61. Steinert, M., Emody, L., Amann, R. & Hacker, J. ( 1997; ). Resuscitation of viable but nonculturable Legionella pneumophila Philadelphia JR32 by Acanthamoeba castellanii. Appl Environ Microbiol 63, 2047–2053.
    [Google Scholar]
  62. Strimmer, K. & von Haeseler, A. ( 1996; ). Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol Biol Evol 13, 964–969.[CrossRef]
    [Google Scholar]
  63. Thao, M. L., Baumann, L., Hess, J. M., Falk, B. W., Ng, J. C., Gullan, P. J. & Baumann, P. ( 2003; ). Phylogenetic evidence for two new insect-associated chlamydia of the family Simkaniaceae. Curr Microbiol 47, 46–50.[CrossRef]
    [Google Scholar]
  64. Visvesvara, G. S. ( 1999; ). Pathogenic and opportunistic free-living amoebae. In Manual of Clinical Microbiology, 7th edn, pp. 1383–1390. Edited by E. J. B. P. R. Murray, M. A. Pfaller, F. C. Tenover & R. H. Yolken. Washington, DC: American Society for Microbiology.
  65. Zhong, G., Fan, P., Ji, H., Dong, F. & Huang, Y. ( 2001; ). Identification of a chlamydial protease-like activity factor responsible for the degradation of host transcription factors. J Exp Med 193, 935–942.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27406-0
Loading
/content/journal/micro/10.1099/mic.0.27406-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error