Microbial Ecology

, Volume 62, Issue 1, pp 134–142 | Cite as

Coxiella Symbionts in the Cayenne Tick Amblyomma cajennense

  • Erik Machado-Ferreira
  • Gabrielle Dietrich
  • Andrias Hojgaard
  • Michael Levin
  • Joseph Piesman
  • Nordin S. Zeidner
  • Carlos A. G. Soares
Invertebrate Microbiology
First Online:
Received:
Accepted:

Abstract

Members of the Coxiella genus are intracellular bacteria that can infect a variety of animals including humans. A symbiotic Coxiella was recently described in Amblyomma americanum ticks in the Northern Hemisphere with no further investigations of other Amblyomma species in other geographic regions. These ixodid ticks represent a group of important vectors for human infectious agents. In the present work, we have demonstrated that symbiotic Coxiella (SCox) are widespread, occurring in South America and infecting 100% of all life stages and eggs of the Cayenne ticks Amblyomma cajennense from Brazil and the USA. Using light microscopy, in situ hybridization, and PCR, we demonstrated SCox in salivary glands, ovaries, and the intestines of A. cajennense. These symbionts are vertically and transtadially transmitted in laboratory reared A. cajennense, and quantitative PCR analyses indicate that SCox are more abundant in adult female ticks, reaching values corresponding to an 11×, 38×, and 200× increase in SCox 16S rRNA gene copy number in unfed females, compared to unfed nymphs, larvae, and eggs, respectively. Phylogenetic analyses showed distinct SCox subpopulations in the USA and Brazil and demonstrated that SCox bacteria do not group with pathogenic Coxiella burnetii.

Keywords

Salivary Gland Symbiotic Bacterium Spotted Fever Coxiella Burnetii Unfed Larva 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
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Notes

Acknowledgments

Erik Machado-Ferreira’s graduate fellowship was supported by the Brazilian federal agency CAPES and by the CDC. This is part of Erik Machado-Ferreira’s PhD thesis work. The authors would like to thank to Mr. Manoel Itamar do Nascimento for tick sampling and Ms. Maria de Fátima S. Cardoso, Mr. Luiz F. P. Frade, and Mr. Sílvio P. Nascimento for their excellent technical assistance. The authors would also like to thank Dr. Robert Massung for his constructive comments.

References

  1. 1.
    Amann RL, Krumholz L, Stahl DA (1990) Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 172:762–770PubMedGoogle Scholar
  2. 2.
    Beare PA, Howe D, Cockrell DC, Omsland A, Hansen B, Hansen RA (2009) Characterization of a Coxiella burnetii ftsZ mutant generated by Himar1 transposon mutagenesis. J Bacteriol 191:1369–1381PubMedCrossRefGoogle Scholar
  3. 3.
    Black W IV, Piesman J (1994) Phylogeny of hard- and soft-tick taxa (Acari: Ixodidae) based on mitochondrial 16S rDNA sequences. Proc Natl Acad Sci USA 91:10034–10038PubMedCrossRefGoogle Scholar
  4. 4.
    Burnevall P, Choucair J, Paraf F, Casalta JP, Raoult D, Scherchen F, Mainardi JL (2001) Detection of fastidious bacteria in cardiac valves in cases of blood culture negative endocardites. J Clin Pathol 54:238–240CrossRefGoogle Scholar
  5. 5.
    Childs JE, Paddock CD (2003) The ascendancy of Amblyomma americanum as a vector of pathogens affecting humans in the United States. Annu Rev Entomol 48:307–337PubMedCrossRefGoogle Scholar
  6. 6.
    Guedes E, Leite RC, Prata MCA, Pacheco RC, Walker DH, Labruna MB (2005) Detection of Rickettsia rickettsii in the tick Amblyomma cajennense in a new Brazilian spotted fever-endemic area in the state of Minas Gerais. Mem Inst Oswaldo Cruz 100:841–845PubMedCrossRefGoogle Scholar
  7. 7.
    Jasinskas A, Zhong J, Barbour A (2007) Highly prevalent Coxiella sp. bacterium in the tick vector Amblyomma americanum. Appl Environ Microbiol 73:334–336PubMedCrossRefGoogle Scholar
  8. 8.
    Klyachko O, Stein BD, Grindle N, Clay K, Fuqua C (2007) Localization and visualization of a Coxiella-type symbiont within the lone star tick, Amblyomma americanum. Appl Environ Microbiol 73:6584–6594PubMedCrossRefGoogle Scholar
  9. 9.
    Labruna MB (2009) Ecology of Rickettsia in South America. Ann NY Acad Sci 1166:156–166PubMedCrossRefGoogle Scholar
  10. 10.
    Lane DJ (1991) 16S/23S rDNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematic. Wiley, New York, pp 115–175Google Scholar
  11. 11.
    Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(delta-delta C(T)) method. Methods 25:402–408PubMedCrossRefGoogle Scholar
  12. 12.
    Machado-Ferreira E, Piesman J, Zeidner NS, Soares CAG (2009) Francisella-like endosymbiont DNA and Francisella tularensis virulence related genes in Brazilian ticks (Acari: Ixodidae). J Med Entomol 46:369–374PubMedCrossRefGoogle Scholar
  13. 13.
    Maurin M, Raoult D (1999) Q fever. Clin Microbiol Rev 12:518–553PubMedGoogle Scholar
  14. 14.
    Park JH, Seok SH, Baek MW, Lee HY, Kim DJ, Cho JS, Kim CK, Hwang DY, Park JH (2006) Microbiological monitoring of guinea pigs reared conventionally at two breeding facilities in Korea. Exp Anim 55:427–432PubMedCrossRefGoogle Scholar
  15. 15.
    Parola P, Raoult D (2001) Ticks and tickborne bacterial diseases in humans: an emerging infectious threat. Clin Infect Dis 32:897–928PubMedCrossRefGoogle Scholar
  16. 16.
    Perlman SJ, Hunter MS, Zchori-Fein E (2006) The emerging diversity of Rickettsia. Proc Biol Sci 273:2097–2106PubMedCrossRefGoogle Scholar
  17. 17.
    Piesman J (1993) Standard system for infecting ticks (Acari:Ixodidae) with the lyme disease spirochete, Borrelia burgdorferi. J Med Entomol 30:199–203PubMedGoogle Scholar
  18. 18.
    Psaroulaki A, Ragiadakou D, Kouris G, Papadopoulus B, Chaniotis B, Tselentis Y (2006) Ticks, tick-borne rickettsiae, and Coxiella burnetii in the Greek Island of Cephalonia. Ann NY Acad Sci 1078:389–399PubMedCrossRefGoogle Scholar
  19. 19.
    Reeves WK, Loftis AD, Sanders F, Spinks MD, Wills W, Denison AM, Dasch GA (2005) Borrelia, Coxiella and Rickettsia in Carios capensis (Acari: Argasidae) from brown pelican (Pelecanus occidentalis) rookery in South Carolina, USA. Exp Appl Acarol 39:321–329CrossRefGoogle Scholar
  20. 20.
    Reeves WK (2008) Molecular evidence for a novel Coxiella from Argas monolakensis (Acari: Argasidae) from Mono Lake, California, USA. Exp Appl Acarol 44:57–60PubMedCrossRefGoogle Scholar
  21. 21.
    Roger F, Roger A (1958) Stain affinities of Rickettsiae & large visible viruses (lymphogranuloma-psittacosis group). I. Mechanism of differentiation with Macchiavello stain & various practical application. Ann Inst Pasteur (Paris) 94:126–128Google Scholar
  22. 22.
    Sanders DM, Parker JE, Walker WW, Buchholz MW, Blount K, Kiel JL (2008) Field collection and genetic classification of tick-borne Rickettsiae and Rickettsiae-like pathogens from south Texas: Coxiella burnetii isolated from field-collected Amblyomma cajennense. Ann NY Acad Sci 1149:208–211PubMedCrossRefGoogle Scholar
  23. 23.
    Smith DJW (1940) Studies of the epidemiology of Q fever. III. The transmission of Q fever by the ticks Haemaphisalis humerosa. Aust J Exp Biol Med Sci 18:103–118CrossRefGoogle Scholar
  24. 24.
    Smith DJW (1941) Studies of the epidemiology of Q fever. VIII. The transmission of Q fever by the ticks Rhipicephalus sanguineus. Aust J Exp Biol Med Sci 19:119–122Google Scholar
  25. 25.
    Smith DJW (1942) Studies of the epidemiology of Q fever. III. The transmission of Q fever by the ticks Ixodes holociclus. Aust J Exp Biol Med Sci 20:213–217CrossRefGoogle Scholar
  26. 26.
    Sonenshine DE (1991) Biology of ticks, vol 1. Oxford University Press, New YorkGoogle Scholar
  27. 27.
    Souza CE, Morales-Fulho J, Ogrzewalska M, Uchoa FC, Horta MC, Souza SS, Borba RC, Labruna MB (2009) Experimental infection of capybaras Hydrochoerus hydrochaeris by Rickettsia rickettsii and evaluation of the transmission of the infection to ticks Amblyomma cajennense. Vet Parasitol 161:116–121PubMedCrossRefGoogle Scholar
  28. 28.
    Troughton DR, Levin ML (2007) Life cycles of seven ixodid tick species (Acari: Ixodidae) under standardized laboratory condition. J Med Entomol 44:732–740PubMedCrossRefGoogle Scholar
  29. 29.
    Zhong J, Jasinskas A, Barbour AG (2007) Antibiotic treatment of the tick vector Amblyomma americanum reduced reproductive fitness. PLoS ONE 2:e405PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Erik Machado-Ferreira
    • 1
    • 2
  • Gabrielle Dietrich
    • 3
  • Andrias Hojgaard
    • 3
  • Michael Levin
    • 3
  • Joseph Piesman
    • 3
  • Nordin S. Zeidner
    • 3
  • Carlos A. G. Soares
    • 1
    • 2
  1. 1.Laboratório de Genética Molecular de Eucariontes e Simbiontes, Dept. Genética, Inst. BiologiaUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  2. 2.Ilha do Fundão, CCSRio de JaneiroBrazil
  3. 3.Division of Vector Borne Diseases, Centers for Disease Control and PreventionFort CollinsUSA

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