1887

Abstract

is a tick-borne rickettsial pathogen that has measurable genetic heterogeneity across its geographical range and reservoir spectrum. In the present study, publicly available sequences of the genes that have prevailingly been used for typing were analysed to identify the segments giving the highest resolution with respect to the predictability of host and geographical provenances of the strains. Selected partial sequences of 16S rRNA, L, 4 and genes were then employed in a tentative multilocus typing scheme used to characterize the strains causing equine granulocytic anaplasmosis (EGA). We were able to both identify alleles characteristic for equine strains of and distinguish two unique genetic variants infecting horses in the Czech Republic. This resolution far exceeded the discriminatory potential of any of the four sequenced genes when used singly. The two novel variants appeared to be phylogenetically closer to the strains reported as causing human disease in Slovenia than to strains thus far isolated from other European EGA cases. A decline in the quality of recently deposited sequences was also demonstrated.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.007831-0
2009-04-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/jmm/58/4/423.html?itemId=/content/journal/jmm/10.1099/jmm.0.007831-0&mimeType=html&fmt=ahah

References

  1. Alberti A., Zobba R., Chessa B., Addis M. F., Spargano O., Parpaglia M. L. P., Cubeddu T., Pintori G., Pittau M. 2005; Equine and canine Anaplasma phagocytophilum strains isolated on the island of Sardinia (Italy) are phylogenetically related to pathogenic strains from United States. Appl Environ Microbiol 71:6418–6422 [CrossRef]
    [Google Scholar]
  2. Ashelford K. E., Chuzhanova N. A., Fry J. C., Jones A. J., Weightman A. J. 2005; At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol 71:7724–7736 [CrossRef]
    [Google Scholar]
  3. Barbet A. F., Lundgren A. M., Alleman A. R., Stuen S., Björnsdorf A., Brown R. N., Drazenovich N. L., Foley J. E. 2006; Structure of the expression site reveals global diversity in MSP2 (P44) variants in Anaplasma phagocytophilum . Infect Immun 74:6429–6437 [CrossRef]
    [Google Scholar]
  4. Bown K. J., Lambin X., Ogden N. H., Petrovec M., Shaw S. E., Woldehiwet Z., Birtles R. J. 2007; High-resolution genetic fingerprinting of European strains of Anaplasma phagocytophilum by use of multilocus variable-number tandem-repeat analysis. J Clin Microbiol 45:1771–1776 [CrossRef]
    [Google Scholar]
  5. Casey A. N. J., Birtles R. J., Radford A. D., Bown K. J., French N. P., Woldehiwet Z., Ogden N. H. 2004; Grouping of highly similar major surface protein (p44)-encoding paralogues: a potential index of genetic diversity amongst isolates of Anaplasma phagocytophilum . Microbiology 150:727–734 [CrossRef]
    [Google Scholar]
  6. Chae J.-S., Foley J. E., Dumler J. S., Madigan J. E. 2000; Comparison of the nucleotide sequences of 16S rRNA, 444 Ep-ank , and groESL heat shock operon genes in naturally occurring Ehrlichia equi and human granulocytic ehrlichiosis agent isolates from Northern California. J Clin Microbiol 38:1364–1369
    [Google Scholar]
  7. Chang Y. F., Novosel V., Dubovi E., Wong S. J., Chu F. K., Chang C. F., Del Piero F., Shin S., Lein D. H. 1998; Experimental infection of the human granulocytic ehrlichiosis agent in horses. Vet Parasitol 78:137–145 [CrossRef]
    [Google Scholar]
  8. Clark A. G., Whittam T. S. 1992; Sequencing errors and molecular evolutionary analysis. Mol Biol Evol 9:744–752
    [Google Scholar]
  9. Clayton R. A., Sutton G., Hinkle P. S. Jr, Bult C., Fields C. 1995; Intraspecific variation in small-subunit rRNA sequences in GenBank: why single sequences may not adequately represent prokaryotic taxa. Int J Syst Bacteriol 45:595–599 [CrossRef]
    [Google Scholar]
  10. De la Fuente J., Massung R. F., Wong S. J., Chu F. K., Lutz H., Meli M., von Loewenich F. D., Grzeszczuk A., Torina A. other authors 2005; Sequence analysis of the msp 4 gene of Anaplasma phagocytophilum strains. J Clin Microbiol 43:1309–1317 [CrossRef]
    [Google Scholar]
  11. Dumler J. S., Barbet A. F., Bekker C. P. J., Dasch G. A., Palmer G. H., Ray S. C., Rikihisa Y., Rurangirwa F. R. 2001; Reorganisation of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales : unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia , descriptions of six new species combinations and designation of Ehrlichia equi and ‘HGE agent’ as subjective synonyms of Ehrlichia phagocytophila . Int J Syst Evol Microbiol 51:2145–2165 [CrossRef]
    [Google Scholar]
  12. Hall T. A. 1999; BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
    [Google Scholar]
  13. Hill F., Gemünd C., Benes V., Ansorge W., Gibson T. J. 2000; An estimate of large-scale sequencing accuracy. EMBO Rep 1:29–31 [CrossRef]
    [Google Scholar]
  14. Hotopp J. C., Lin M., Madupu R., Grabtree J., Angiuoli S. V., Eisen J., Seshadri R., Ren Q., Wu M. other authors 2006; Comparative genomics of emerging human ehrlichiosis agents. PLoS Genet 2:e21 [CrossRef]
    [Google Scholar]
  15. Ijdo J. W., Carlson A. C., Kennedy E. L. 2007; Anaplasma phagocytophilum AnkA is tyrosine-phosphorylated at EPIYA motifs and recruits SHP-1 during early infection. Cell Microbiol 9:1284–1296 [CrossRef]
    [Google Scholar]
  16. Johansson K.-E., Pettersson B., Uhlén M., Gunnarsson A., Malmquist M., Olsson E. 1995; Identification of the causative agent of granulocytic ehrlichiosis in Swedish dogs and horses by direct solid phase sequencing of PCR products from the 16S rRNA gene. Res Vet Sci 58:109–112 [CrossRef]
    [Google Scholar]
  17. Kim H.-Y., Mott J., Zhi N., Tajima T., Rikihisa Y. 2002; Cytokine gene expression by peripheral blood leucocytes in horses experimentally infected with Anaplasma phagocytophila . Clin Diagn Lab Immunol 9:1079–1084
    [Google Scholar]
  18. Lewis G. E., Huxsoll D. L., Ristic M., Johnson A. J. 1975; Experimentally induced infection of dogs, cats, and nonhuman primates with Ehrlichia equi , etiologic agent of equine ehrlichiosis. Am J Vet Res 36:85–88
    [Google Scholar]
  19. Lin Q., Rikihisa Y., Massung R. F., Woldehiwet Z., Falco R. C. 2004; Polymorphism and transcription at the p44–1/p44–18 genomic locus in Anaplasma phagocytophilum strains from diverse geographic regions. Infect Immun 72:5574–5581 [CrossRef]
    [Google Scholar]
  20. Madigan J. E., Richter P. J. Jr, Kimsey R. B., Barlough J. E., Bakken J. S., Dumler J. S. 1995; Transmission and passage in horses of the agent of human granulocytic ehrlichiosis. J Infect Dis 172:1141–1144 [CrossRef]
    [Google Scholar]
  21. Madigan J. E., Barlough J. E., Dumler J. S., Schankmann N. S., DeRock E. 1996; Equine granulocytic ehrlichiosis in Connecticut caused by an agent resembling the human granulocytotrophic ehrlichia. J Clin Microbiol 34:434–435
    [Google Scholar]
  22. Maiden M. C. J., Bygraves J. A., Feil E., Morelli G., Russel J. E., Urwin R., Zhang Q., Zhou J., Zurth K. other authors 1998; Multicocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A 95:3140–3145 [CrossRef]
    [Google Scholar]
  23. Massung R. F., Slater K., Owens J. H., Nicholson W. L., Mather T. N., Solberg V. B., Olson J. G. 1998; Nested PCR assay for detection of granulocytic ehrlichiae. J Clin Microbiol 36:1090–1095
    [Google Scholar]
  24. Massung R. F., Owens J. H., Ross D., Reed K. D., Petrovec M., Bjoersdorff A., Coughlin R. T., Beltz G. A., Murphy C. I. 2000; Sequence analysis of the ank gene of granulocytic ehrlichiae. J Clin Microbiol 38:2917–2922
    [Google Scholar]
  25. Massung R. F., Mauel M. J., Owens J. H., Allan N., Courtney J. W., Stafford K. C., Mather T. N. 2002; Genetic variants of Ehrlichia phagocytophila , Rhode Island and Connecticut. Emerg Infect Dis 8:467–472 [CrossRef]
    [Google Scholar]
  26. Massung R. F., Courtney J. W., Hiratzka S. L., Pitzer V. E., Smith G., Dryden R. L. 2005; Anaplasma phagocytophilum in white-tailed deer. Emerg Infect Dis 11:1604–1606 [CrossRef]
    [Google Scholar]
  27. Masuzawa T., Kharitonenkov I. G., Okamoto Y., Fukui T., Ohashi N. 2008; Prevalence of Anaplasma phagocytophilum and its coinfection with Borrelia afzelii in Ixodes ricinus and Ixodes persulcatus ticks inhabiting Tver Province (Russia) – a sympatric region for both tick species. J Med Microbiol 57:986–991 [CrossRef]
    [Google Scholar]
  28. Mathews D. H., Disney M. D., Childs J. L., Schroeder S. J., Zuker M., Turner D. H. 2004; Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc Natl Acad Sci U S A 101:7287–7292 [CrossRef]
    [Google Scholar]
  29. Ohashi N., Inayoshi M., Kitamura K., Kawamori F., Kawaguchi D., Nishimura Y., Naitou H., Hiroi M., Masuzawa T. 2005; Anaplasma phagocytophilum -infected ticks, Japan. Emerg Infect Dis 11:1780–1783 [CrossRef]
    [Google Scholar]
  30. Olsson-Engvall E., Pettersson B., Persson M., Artursson K., Johansson K.-E. 1996; A 16S rRNA-based PCR assay for detection and identification of granulocytic Ehrlichia species in dogs, horses, and cattle. J Clin Microbiol 34:2170–2174
    [Google Scholar]
  31. Perez-Losada M., Browne E. B., Madsen A., Wirth T., Viscidi R. P., Crandall K. A. 2006; Population genetics of microbial pathogens estimated from multilocus sequence typing (MLST) data. Infect Genet Evol 6:97–112 [CrossRef]
    [Google Scholar]
  32. Press W. H., Teukolsky S. A., Vetterling W. T., Flannery B. P. 1992 Numerical Recipes in C: the Art of Scientific Computing , 2nd edn. New York: Cambridge University Press;
    [Google Scholar]
  33. Pusterla N., Hudler J. B., Feige K., Lutz H. 1998; Identification of a granulocytic Ehrlichia strain isolated from a horse in Switzerland and comparison with other rickettsiae of the Ehrlichia phagocytophila genogroup. J Clin Microbiol 36:2035–2037
    [Google Scholar]
  34. Pusterla N., Leutenegger C. M., Chae J.-S., Lutz H., Kimsley R. B., Dumler J. S., Madigan J. E. 1999a; Quantitative evaluation of ehrlichial burden in horses after experimental transmission of human granulocytic Ehrlichia agent by intravenous inoculation with infected leucocytes and infected ticks. J Clin Microbiol 37:4042–4044
    [Google Scholar]
  35. Pusterla N., Pusterla J. B., Braun U., Lutz H. 1999b; Experimental cross-infections with Ehrlichia phagocytophila and human granulocytic ehrlichia-like agent in cows and horses. Vet Rec 145:311–314 [CrossRef]
    [Google Scholar]
  36. Pusterla N., Anderson R. J., House J. K., Pusterla J. B., DeRock E., Madigan J. E. 2001; Susceptibility of cattle to infection with Ehrlichia equi and the agent of human granulocytic ehrlichiosis. J Am Vet Med Assoc 218:1160–1162 [CrossRef]
    [Google Scholar]
  37. Richterich P. 1998; Estimation of errors in “raw” DNA sequences: a validation study. Genome Res 8:251–259 [CrossRef]
    [Google Scholar]
  38. Rost B., Yachdav G., Liu J. 2004; The PredictProtein server. Nucleic Acids Research 32:W321–W326 [CrossRef]
    [Google Scholar]
  39. Schneider T. D., Stephens R. M. 1990; Sequence logos: a new way to display consensus sequences. Nucleic Acids Res 18:6097–6100 [CrossRef]
    [Google Scholar]
  40. Shukla S. K., Aswani V., Stockwell P. J., Reed K. D. 2007; Contribution of polymorphisms in ankA, gltA , and groESL in defining genetic variants of Anaplasma phagocytophilum . J Clin Microbiol 45:2312–2315 [CrossRef]
    [Google Scholar]
  41. Stuen S., Artursson K., Olsson-Engvall E. 1998; Experimental infection of lambs with an equine granulocytic Ehrlichia species resembling the agent that causes human granulocytic ehrlichiosis (HGE). Acta Vet Scand 39:491–497
    [Google Scholar]
  42. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: 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]
  43. Urwin R., Maiden M. C. J. 2003; Multi-locus sequence typing: a tool for global epidemiology. Trends Microbiol 11:479–487 [CrossRef]
    [Google Scholar]
  44. Von Loewenich F. D., Baumgartner B. U., Schroppel K., Geisdorfer W., Rollinghof M., Bogdan C. 2003; High diversity of ankA sequences of Anaplasma phagocytophilum among Ixodes ricinus ticks in Germany. J Clin Microbiol 41:5033–5040 [CrossRef]
    [Google Scholar]
  45. Wesche P. L., Gaffney D. J., Keightley P. D. 2004; DNA sequence error rates in GenBank records estimated using the mouse genome as a reference. DNA Seq 15:362–364
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.007831-0
Loading
/content/journal/jmm/10.1099/jmm.0.007831-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

PDF

Supplementary material 3

PDF
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