Skip to main content
Applied and Environmental Microbiology logoLink to Applied and Environmental Microbiology
. 1997 Oct;63(10):3926–3932. doi: 10.1128/aem.63.10.3926-3932.1997

Endosymbionts of ticks and their relationship to Wolbachia spp. and tick-borne pathogens of humans and animals.

H Noda 1, U G Munderloh 1, T J Kurtti 1
PMCID: PMC168704  PMID: 9327557

Abstract

The presence, internal distribution, and phylogenetic position of endosymbiotic bacteria from four species of specific-pathogen-free ticks were studied. These included the hard ticks Ixodes scapularis (the black-legged tick), Rhipicephalus sanguineus (the brown dog tick), and Haemaphysalis longicornis and the African soft tick Ornithodoros moubata. PCR assays for bacteria, using two sets of general primers for eubacterial 16S and 23S rRNA genes (rDNAs) and seven sets of specific primers for wolbachial, rickettsial, or Francisella genes, indicated that I. scapularis possessed symbiotic rickettsiae in the ovaries and that the other species harbored eubacteria in both the ovaries and Malpighian tubules. Phylogenetic analysis based on the sequence of 16S rDNA indicated that the symbiont of I. scapularis belonged to the alpha subgroup of proteobacteria and was closely related to the members of the genus Rickettsia. The other species had similar microorganisms in the ovaries and Malpighian tubules, which belonged to the gamma subgroup of proteobacteria, and formed a monophyletic group with the Q-fever pathogen, Coxiella burnetii. O. moubata harbored another symbiont, which formed a monophyletic group with Francisella tularensis and Wolbachia persica, the latter a symbiont previously isolated from Malpighian tubules of the soft tick Argas (Persicargas) arboreus. Thus, the symbionts of these four tick species were not related to the Wolbachia species found in insects. The two symbionts that live in the Malpighian tubules, one closely related to C. burnetii and the other closely related to F. tularensis, appear to be of ancient origin and be widely distributed in ticks.

Full Text

The Full Text of this article is available as a PDF (1.3 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Akporiaye E. T., Rowatt J. D., Aragon A. A., Baca O. G. Lysosomal response of a murine macrophage-like cell line persistently infected with Coxiella burnetii. Infect Immun. 1983 Jun;40(3):1155–1162. doi: 10.1128/iai.40.3.1155-1162.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BURGDORFER W., OWEN C. R. Experimental studies on argasid ticks as possible vectors of tularemia. J Infect Dis. 1956 Jan-Feb;98(1):67–74. doi: 10.1093/infdis/98.1.67. [DOI] [PubMed] [Google Scholar]
  3. Baca O. G., Paretsky D. Q fever and Coxiella burnetii: a model for host-parasite interactions. Microbiol Rev. 1983 Jun;47(2):127–149. doi: 10.1128/mr.47.2.127-149.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Breeuwer J. A., Jacobs G. Wolbachia: intracellular manipulators of mite reproduction. Exp Appl Acarol. 1996 Aug;20(8):421–434. doi: 10.1007/BF00053306. [DOI] [PubMed] [Google Scholar]
  5. Burgdorfer W., Brinton L. P., Hughes L. E. Isolation and characterization of symbiotes from the Rocky Mountain wood tick, Dermacentor andersoni. J Invertebr Pathol. 1973 Nov;22(3):424–434. doi: 10.1016/0022-2011(73)90173-0. [DOI] [PubMed] [Google Scholar]
  6. Burton P. R., Kordová N., Paretsky D. Electron microscopic studies of the rickettsia Coxiella burneti: entry, lysosomal response, and fate of rickettsial DNA in L-cells. Can J Microbiol. 1971 Feb;17(2):143–150. doi: 10.1139/m71-025. [DOI] [PubMed] [Google Scholar]
  7. Forsman M., Sandström G., Sjöstedt A. Analysis of 16S ribosomal DNA sequences of Francisella strains and utilization for determination of the phylogeny of the genus and for identification of strains by PCR. Int J Syst Bacteriol. 1994 Jan;44(1):38–46. doi: 10.1099/00207713-44-1-38. [DOI] [PubMed] [Google Scholar]
  8. Frothingham R., Allen R. L., Wilson K. H. Rapid 16S ribosomal DNA sequencing from a single colony without DNA extraction or purification. Biotechniques. 1991 Jul;11(1):40–44. [PubMed] [Google Scholar]
  9. Gage K. L., Gilmore R. D., Karstens R. H., Schwan T. G. Detection of Rickettsia rickettsii in saliva, hemolymph and triturated tissues of infected Dermacentor andersoni ticks by polymerase chain reaction. Mol Cell Probes. 1992 Aug;6(4):333–341. doi: 10.1016/0890-8508(92)90010-u. [DOI] [PubMed] [Google Scholar]
  10. Hayes S. F., Burgdorfer W. Ultrastructure of Rickettsia rhipicephali, a new member of the spotted fever group rickettsiae in tissues of the host vector Rhipicephalus sanguineus. J Bacteriol. 1979 Jan;137(1):605–613. doi: 10.1128/jb.137.1.605-613.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Holden P. R., Brookfield J. F., Jones P. Cloning and characterization of an ftsZ homologue from a bacterial symbiont of Drosophila melanogaster. Mol Gen Genet. 1993 Aug;240(2):213–220. doi: 10.1007/BF00277059. [DOI] [PubMed] [Google Scholar]
  12. Lane D. J., Pace B., Olsen G. J., Stahl D. A., Sogin M. L., Pace N. R. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci U S A. 1985 Oct;82(20):6955–6959. doi: 10.1073/pnas.82.20.6955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lewis D. The detection of rickettsia-like microorganisms within the ovaries of female Ixodes ricinus ticks. Z Parasitenkd. 1979 Sep;59(3):295–298. doi: 10.1007/BF00927523. [DOI] [PubMed] [Google Scholar]
  14. Magnarelli L. A., Andreadis T. G., Stafford K. C., 3rd, Holland C. J. Rickettsiae and Borrelia burgdorferi in ixodid ticks. J Clin Microbiol. 1991 Dec;29(12):2798–2804. doi: 10.1128/jcm.29.12.2798-2804.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. McCaul T. F., Williams J. C. Developmental cycle of Coxiella burnetii: structure and morphogenesis of vegetative and sporogenic differentiations. J Bacteriol. 1981 Sep;147(3):1063–1076. doi: 10.1128/jb.147.3.1063-1076.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Munderloh U. G., Liu Y., Wang M., Chen C., Kurtti T. J. Establishment, maintenance and description of cell lines from the tick Ixodes scapularis. J Parasitol. 1994 Aug;80(4):533–543. [PubMed] [Google Scholar]
  17. O'Neill S. L., Giordano R., Colbert A. M., Karr T. L., Robertson H. M. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):2699–2702. doi: 10.1073/pnas.89.7.2699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Regnery R. L., Spruill C. L., Plikaytis B. D. Genotypic identification of rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. J Bacteriol. 1991 Mar;173(5):1576–1589. doi: 10.1128/jb.173.5.1576-1589.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Reinhardt C., Aeschlimann A., Hecker H. Distribution of Rickettsia-like microorganisms in various organs of an Ornithodorus moubata laboratory strain (Ixodoidea, Argasidae) as revealed by electron microscopy. Z Parasitenkd. 1972;39(3):201–209. doi: 10.1007/BF00329456. [DOI] [PubMed] [Google Scholar]
  20. Roshdy M. A. A rickettsialike microorganism in the tick Ornithodoros savignyi: Observations on its structure and distribution in the tissues of the tick. J Invertebr Pathol. 1968 Aug;11(2):155–169. doi: 10.1016/0022-2011(68)90146-8. [DOI] [PubMed] [Google Scholar]
  21. Rousset F., Bouchon D., Pintureau B., Juchault P., Solignac M. Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proc Biol Sci. 1992 Nov 23;250(1328):91–98. doi: 10.1098/rspb.1992.0135. [DOI] [PubMed] [Google Scholar]
  22. Rousset F., Vautrin D., Solignac M. Molecular identification of Wolbachia, the agent of cytoplasmic incompatibility in Drosophila simulans, and variability in relation with host mitochondrial types. Proc Biol Sci. 1992 Mar 23;247(1320):163–168. doi: 10.1098/rspb.1992.0023. [DOI] [PubMed] [Google Scholar]
  23. Smith R. D., Sells D. M., Stephenson E. H., Ristic M. R., Huxsoll D. L. Development of Ehrlichia canis, causative agent of canine ehrlichiosis, in the tick Rhipicephalus sanguineus and its differentiation from a symbiotic Rickettsia. Am J Vet Res. 1976 Feb;37(2):119–126. [PubMed] [Google Scholar]
  24. Sutáková G., Rehácek J. Endocytobionts in Dermacentor reticulatus ticks (Ixodidae): an electron microscope study. Exp Appl Acarol. 1991 Apr;11(1):57–72. doi: 10.1007/BF01193729. [DOI] [PubMed] [Google Scholar]
  25. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tsagkarakou A., Guillemaud T., Rousset F., Navajas M. Molecular identification of a Wolbachia endosymbiont in a Tetranychus urticae strain (Acari: Tetranychidae). Insect Mol Biol. 1996 Aug;5(3):217–221. doi: 10.1111/j.1365-2583.1996.tb00057.x. [DOI] [PubMed] [Google Scholar]
  27. Weisburg W. G., Barns S. M., Pelletier D. A., Lane D. J. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol. 1991 Jan;173(2):697–703. doi: 10.1128/jb.173.2.697-703.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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. Phylogenetic diversity of the Rickettsiae. J Bacteriol. 1989 Aug;171(8):4202–4206. doi: 10.1128/jb.171.8.4202-4206.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Williams S. G., Sacci J. B., Jr, Schriefer M. E., Andersen E. M., Fujioka K. K., Sorvillo F. J., Barr A. R., Azad A. F. Typhus and typhuslike rickettsiae associated with opossums and their fleas in Los Angeles County, California. J Clin Microbiol. 1992 Jul;30(7):1758–1762. doi: 10.1128/jcm.30.7.1758-1762.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Woese C. R. Bacterial evolution. Microbiol Rev. 1987 Jun;51(2):221–271. doi: 10.1128/mr.51.2.221-271.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Yano Y., Takada N., Fujita H. Ultrastructure of spotted fever rickettsialike microorganisms observed in tissues of Dermacentor taiwanensis (Acari: Ixodidae). J Med Entomol. 1993 May;30(3):579–585. doi: 10.1093/jmedent/30.3.579. [DOI] [PubMed] [Google Scholar]
  32. el Shoura S. M. Ultrastructure and distribution of intracellular rickettsia-like microorganisms in various organs of the laboratory-reared adult tick Argas (Persicargas) arboreus (Ixodoidea: Argasidae). Exp Appl Acarol. 1990 Aug;9(1-2):137–143. doi: 10.1007/BF01198992. [DOI] [PubMed] [Google Scholar]

Articles from Applied and Environmental Microbiology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES