1887

Abstract

In 1911, Sir Arnold Theiler isolated and described a parasite that was very similar to Anaplasma marginale but which was more centrally located within the erythrocytes of the host cells, and was much less pathogenic than A. marginale . He named the parasite A. marginale variety centrale. The name Anaplasma centrale , referring to the same organism, was published in Validation List No. 15 in 1984, but the publication was based on an erroneous assumption that Theiler had indicated that it was a separate species. Many authors have subsequently accepted this organism as a separate species, but evidence to indicate that it is a distinct species has never been presented. The near full-length 16S rRNA gene sequence, and the deduced amino acid sequences for groEL and msp4 from several isolates of A. marginale and A. centrale from around South Africa were compared with those of the A. marginale type strain, St Maries, and the A. centrale Israel strain and other reference sequences. Phylogenetic analyses of these sequences demonstrated that A. centrale consistently forms a separate clade from A. marginale , supported by high bootstrap values (≥90 %), revealing that there is divergence between these two organisms. In addition, we discuss distinctive characteristics which have been published recently, such as differences in Msp1a/Msp1aS gene structure, as well as genome architecture that provide further evidence to suggest that A. centrale is, in fact, a separate species. Our results, therefore, provide evidence to support the existing nomenclature, and confirm that A. centrale (ex Theiler 1911) Ristic and Kreier 1984 is, indeed, a distinct species.

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2018-06-19
2024-04-19
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References

  1. Salmon DE, Smith T. Infectious diseases of cattle: southern cattle fever (Texas fever). In Special Report on Diseases of Cattle and on Cattle Feeding USDA Bureau of Animal Industry Washington: Government Printing Office; 1896 pp. 428–438
    [Google Scholar]
  2. Theiler A. Anaplasma marginale: the marginal points in the blood of cattle suffering from a specific disease. In Report to the Government, Transvaal, South Africa Veterinary Bacteriology, Dept. of Agriculture 1908-9 1910 pp. 7–64
    [Google Scholar]
  3. Theiler A. Further investigations into anaplasmosis of South African cattle. In First Report of the Director of Veterinary Research Union of South Africa 1911 pp. 7–46
    [Google Scholar]
  4. Inokuma H, Terada Y, Kamio T, Raoult D, Brouqui P. Analysis of the 16S rRNA gene sequence of Anaplasma centrale and its phylogenetic relatedness to other ehrlichiae. Clin Diagn Lab Immunol 2001; 8:241–244 [View Article][PubMed]
    [Google Scholar]
  5. Shkap V, Molad T, Brayton KA, Brown WC, Palmer GH. Expression of major surface protein 2 variants with conserved T-cell epitopes in Anaplasma centrale vaccinates. Infect Immun 2002; 70:642–648 [View Article][PubMed]
    [Google Scholar]
  6. Lew AE, Bock RE, Minchin CM, Masaka S. A msp1 alpha polymerase chain reaction assay for specific detection and differentiation of Anaplasma marginale isolates. Vet Microbiol 2002; 86:325–335 [View Article][PubMed]
    [Google Scholar]
  7. Kocan KM, de La Fuente J, Guglielmone AA, Meléndez RD. Antigens and alternatives for control of Anaplasma marginale infection in cattle. Clin Microbiol Rev 2003; 16:698–712 [View Article][PubMed]
    [Google Scholar]
  8. Carelli G, Decaro N, Lorusso A, Elia G, Lorusso E et al. Detection and quantification of Anaplasma marginale DNA in blood samples of cattle by real-time PCR. Vet Microbiol 2007; 124:107–114 [View Article][PubMed]
    [Google Scholar]
  9. Mtshali MS, de La Fuente J, Ruybal P, Kocan KM, Vicente J et al. Prevalence and genetic diversity of Anaplasma marginale strains in cattle in South Africa. Zoonoses Public Health 2007; 54:23–30 [View Article][PubMed]
    [Google Scholar]
  10. Carelli G, Decaro N, Lorusso E, Paradies P, Elia G et al. First report of bovine anaplasmosis caused by Anaplasma centrale in Europe. Ann N Y Acad Sci 2008; 1149:107–110 [View Article][PubMed]
    [Google Scholar]
  11. Decaro N, Carelli G, Lorusso E, Lucente MS, Greco G et al. Duplex real-time polymerase chain reaction for simultaneous detection and quantification of Anaplasma marginale and Anaplasma centrale. J Vet Diagn Invest 2008; 20:606–611 [View Article][PubMed]
    [Google Scholar]
  12. Rymaszewska A, Grenda S. Bacteria of the genus Anaplasma–characteristics of Anaplasma and their vectors: a review. Vet Med 2008; 53:573–584
    [Google Scholar]
  13. Aubry P, Geale DW. A review of bovine anaplasmosis. Transbound Emerg Dis 2011; 58:1–30 [View Article][PubMed]
    [Google Scholar]
  14. Bell-Sakyi L, Palomar AM, Bradford EL, Shkap V. Propagation of the Israeli vaccine strain of Anaplasma centrale in tick cell lines. Vet Microbiol 2015; 179:270–276 [View Article][PubMed]
    [Google Scholar]
  15. Ristic M. Anaplasmosis. In Weinman D, Ristic D. (editors) Infectious Blood Diseases of Man and Animals New York, USA: Academic Press; 1968 pp. 473–542
    [Google Scholar]
  16. International Journal of Systematic and Bacteriology Validation of the publication of new names and new combinations previously effectively published outside the IJSB list no.15. IUMS 1984; 34:355–357
    [Google Scholar]
  17. Ristic M, Kreier JP. Family. III. Anaplasmataceae Philip 1957, 980AL. In Krieg NR, Holt JG. (editors) Bergey’s Manual of Systematic Bacteriology Baltimore: Williams & Wilkins; 1984 pp. 719–729
    [Google Scholar]
  18. Dumler JS, Barbet AF, Bekker CP, Dasch GA, Palmer GH et al. Reorganization 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 2001; 51:2145–2165 [View Article][PubMed]
    [Google Scholar]
  19. Brayton KA, Dark MJ. Anaplasma. In Nene V, Kole C. (editors) Genome Mapping and Genomics in Animal-Associated Microbes Berlin/Heidelberg, Germany: Springer; 2009 pp. 85–116
    [Google Scholar]
  20. Khumalo ZT, Catanese HN, Liesching N, Hove P, Collins NE et al. Characterization of Anaplasma marginale subsp. centrale strains by use of msp1aS genotyping reveals a wildlife reservoir. J Clin Microbiol 2016; 54:2503–2512 [View Article][PubMed]
    [Google Scholar]
  21. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article][PubMed]
    [Google Scholar]
  22. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002; 30:3059–3066 [View Article][PubMed]
    [Google Scholar]
  23. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1999; 41:95–98
    [Google Scholar]
  24. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article][PubMed]
    [Google Scholar]
  25. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article][PubMed]
    [Google Scholar]
  26. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003; 19:1572–1574 [View Article][PubMed]
    [Google Scholar]
  27. Abascal F, Zardoya R, Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005; 21:2104–2105 [View Article][PubMed]
    [Google Scholar]
  28. Posada D, Crandall KA. ModelTest: testing the model of DNA substitution. Bioinformatics 1998; 14:817–818 [View Article][PubMed]
    [Google Scholar]
  29. Sisson D, Hufschmid J, Jolles A, Beechler B, Jabbar A. Molecular characterisation of Anaplasma species from African buffalo (Syncerus caffer) in Kruger National Park, South Africa. Ticks Tick Borne Dis 2017; 8:400–406 [View Article][PubMed]
    [Google Scholar]
  30. Lew AE, Gale KR, Minchin CM, Shkap V, de Waal DT. Phylogenetic analysis of the erythrocytic Anaplasma species based on 16S rDNA and GroEL (HSP60) sequences of A. marginale, A. centrale, and A. ovis and the specific detection of A. centrale vaccine strain. Vet Microbiol 2003; 92:145–160 [View Article][PubMed]
    [Google Scholar]
  31. Liu Z, Luo J, Bai Q, Ma M, Guan G et al. Amplification of 16S rRNA genes of Anaplasma species in China for phylogenetic analysis. Vet Microbiol 2005; 107:145–148 [View Article][PubMed]
    [Google Scholar]
  32. Yang J, Liu Z, Niu Q, Liu J, Han R et al. A novel zoonotic Anaplasma species is prevalent in small ruminants: potential public health implications. Parasit Vectors 2017; 10:1–6 [View Article][PubMed]
    [Google Scholar]
  33. Li H, Zheng YC, Ma L, Jia N, Jiang BG et al. Human infection with a novel tick-borne Anaplasma species in China: a surveillance study. Lancet Infect Dis 2015; 15:663–670 [View Article][PubMed]
    [Google Scholar]
  34. Palmer GH, Barbet AF, Musoke AJ, Katende JM, Rurangirwa F et al. Recognition of conserved surface protein epitopes on Anaplasma centrale and Anaplasma marginale isolates from Israel, Kenya and the United States. Int J Parasitol 1988; 18:33–38 [View Article][PubMed]
    [Google Scholar]
  35. Visser ES, Ambrosio RE, de Waal DT. An Anaplasma centrale DNA probe that differentiates between Anaplasma ovis and Anaplasma marginale DNA. Vet Microbiol 1991; 28:313–325 [View Article][PubMed]
    [Google Scholar]
  36. Ngeranwa JJ, Venter EH, Penzhorn BL, Soi RK, Mwanzia J et al. Characterization of Anaplasma isolates from eland (Taurotragus oryx). Pathogenicity in cattle and sheep and DNA profiles analysis. Vet Parasitol 1998; 74:109–122[PubMed]
    [Google Scholar]
  37. de La Fuente J, Massung RF, Wong SJ, Chu FK, Lutz H et al. Sequence analysis of the msp4 gene of Anaplasma phagocytophilum strains. J Clin Microbiol 2005; 43:1309–1317 [View Article][PubMed]
    [Google Scholar]
  38. Zhan L, Cao WC, Jiang JF, Zhang XA, Liu YX et al. Anaplasma phagocytophilum from rodents and sheep, China. Emerg Infect Dis 2010; 16:764–768 [View Article][PubMed]
    [Google Scholar]
  39. Bruner DW, Gillespie JH. Hagan's Infectious Diseases of Domestic Animals vol. 5 Ithaca, New York: Comstock; 1966 pp. 344
    [Google Scholar]
  40. Henning MW. Animal diseases in South Africa, 3rd ed. South Africa: Central News Agency Ltd; 1949 pp. 398
    [Google Scholar]
  41. Waddell AH. Observations on the morphology of Anaplasma centrale. Aust Vet J 1964; 40:53–54 [View Article]
    [Google Scholar]
  42. Shkap V, Pipano E, McGuire TC, Palmer GH. Identification of immunodominant polypeptides common between Anaplasma centrale and Anaplasma marginale. Vet Immunol Immunopathol 1991; 29:31–40 [View Article][PubMed]
    [Google Scholar]
  43. Agnes JT, Brayton KA, Lafollett M, Norimine J, Brown WC et al. Identification of Anaplasma marginale outer membrane protein antigens conserved between A. marginale sensu stricto strains and the live A. marginale subsp. centrale vaccine. Infect Immun 2011; 79:1311–1318 [View Article][PubMed]
    [Google Scholar]
  44. Kocan KM, de La Fuente J, Blouin EF, Coetzee JF, Ewing SA. The natural history of Anaplasma marginale. Vet Parasitol 2010; 167:95–107 [View Article][PubMed]
    [Google Scholar]
  45. de Waal DT. Anaplasmosis control and diagnosis in South Africa. Ann N Y Acad Sci 2000; 916:474–483 [View Article][PubMed]
    [Google Scholar]
  46. Shkap V, Kocan K, Molad T, Mazuz M, Leibovich B et al. Experimental transmission of field Anaplasma marginale and the A. centrale vaccine strain by Hyalomma excavatum, Rhipicephalus sanguineus and Rhipicephalus (Boophilus) annulatus ticks. Vet Microbiol 2009; 134:254–260 [View Article][PubMed]
    [Google Scholar]
  47. Potgieter FT, van Rensburg L. Tick transmission of Anaplasma centrale. Onderstepoort J Vet Res 1987; 54:5–7[PubMed]
    [Google Scholar]
  48. Ueti MW, Knowles DP, Davitt CM, Scoles GA, Baszler TV et al. Quantitative differences in salivary pathogen load during tick transmission underlie strain-specific variation in transmission efficiency of Anaplasma marginale. Infect Immun 2009; 77:70–75 [View Article][PubMed]
    [Google Scholar]
  49. Herndon DR, Palmer GH, Shkap V, Knowles DP, Brayton KA. Complete genome sequence of Anaplasma marginale subsp. centrale. J Bacteriol 2010; 192:379–380 [View Article][PubMed]
    [Google Scholar]
  50. Brayton KA, Kappmeyer LS, Herndon DR, Dark MJ, Tibbals DL et al. Complete genome sequencing of Anaplasma marginale reveals that the surface is skewed to two superfamilies of outer membrane proteins. Proc Natl Acad Sci USA 2005; 102:844–849 [View Article][PubMed]
    [Google Scholar]
  51. Dark MJ, Herndon DR, Kappmeyer LS, Gonzales MP, Nordeen E et al. Conservation in the face of diversity: multistrain analysis of an intracellular bacterium. BMC Genomics 2009; 10:16 [View Article][PubMed]
    [Google Scholar]
  52. Debeila EM. Occurrence of Anaplasma and Ehrlichia Species in African Buffalo (Syncerus caffer) in Kruger National Park and Hluhluwe-Imfolozi Park in South Africa MSc dissertation Department of Veterinary Tropical Diseases, University of Pretoria, Pretoria, South Africa; 2012
    [Google Scholar]
  53. Mutshembele AM, Cabezas-Cruz A, Mtshali MS, Thekisoe OM, Galindo RC et al. Epidemiology and evolution of the genetic variability of Anaplasma marginale in South Africa. Ticks Tick Borne Dis 2014; 5:624–631 [View Article][PubMed]
    [Google Scholar]
  54. Oura CA, Tait A, Asiimwe B, Lubega GW, Weir W. Haemoparasite prevalence and Theileria parva strain diversity in Cape buffalo (Syncerus caffer) in Uganda. Vet Parasitol 2011; 175:212–219 [View Article][PubMed]
    [Google Scholar]
  55. Eygelaar D, Jori F, Mokopasetso M, Sibeko KP, Collins NE et al. Tick-borne haemoparasites in African buffalo (Syncerus caffer) from two wildlife areas in Northern Botswana. Parasit Vectors 2015; 8:26 [View Article][PubMed]
    [Google Scholar]
  56. Palomar AM, Portillo A, Santibáñez P, Mazuelas D, Roncero L et al. Detection of tick-borne Anaplasma bovis, Anaplasma phagocytophilum and Anaplasma centrale in Spain. Med Vet Entomol 2015; 29:349–353 [View Article][PubMed]
    [Google Scholar]
  57. Joazeiro AC, Martins J, Masuda A, Seixas A, Junior I. A PCR for differentiate between Anaplasma marginale and A. centrale. Acta Sci Vet 2015; 43:1270
    [Google Scholar]
  58. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 1991; 173:697–703 [View Article][PubMed]
    [Google Scholar]
  59. List of Prokaryotic Names with Standing in Nomenclature Last updated in 2015 www.bacterio.net/anaplasma.html Last viewed on the 27 March 2018
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