Clonal origin of emerging populations of Ehrlichia ruminantium in Burkina Faso

Infection, Genetics and Evolution

Volumn 10, Issue 7, 2010, Pages 903-912

  Adakal, Hassane ^a,b   Gavotte, Laurent ^c   Stachurski, Frédéric ^b   Konkobo, Maurice ^a   Henri, Hélène ^d,e,f   Zoungrana, Sébastien ^a   Huber, Karine ^b   Vachiery, Nathalie ^b   Martinez, Dominique ^b   Morand, Serge ^c   Frutos, Roger ^g  

^a CIRDES Laboratoire de Biotechnologie (URBIO)   (France)

^b CIRAD   (France)

^c INSTITUT DES SCIENCES DE L EVOLUTION   (France)

^d UNIVERSITÉ DE LYON   (France)

^e UNIVERSITÉ LYON 1   (France)

^f LABORATOIRE DE BIOMÉTRIE ET BIOLOGIE EVOLUTIVE   (France)

^g INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

Ehrlichia ruminantium; Emergence; Genetic diversity; Genomic stasis; MLST; Phylogeny; Polymorphism; Recombination

Indexed keywords

BACTERIAL DNA;

AFRICA; ARTICLE; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL STRAIN; CENTRAL AMERICA; CLONAL VARIATION; CONTROLLED STUDY; DNA POLYMORPHISM; DNA SEQUENCE; EHRLICHIA RUMINANTIUM; EVOLUTION; FRANCE; GENE FUNCTION; GENE MUTATION; GENETIC VARIABILITY; GENOME ANALYSIS; GLTA GENE; GROEL GENE; LEPA GENE; LIPA GENE; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NUCLEOTIDE SEQUENCE; PREVALENCE; PRIORITY JOURNAL; SECY GENE; SEQUENCE ANALYSIS; SODB GENE; SOUTH AFRICA; STRAIN DIFFERENCE; SUCA GENE;

ANIMALS; BURKINA FASO; EHRLICHIA RUMINANTIUM; EVOLUTION, MOLECULAR; HAPLOTYPES; IXODIDAE; LINKAGE DISEQUILIBRIUM; POLYMORPHISM, GENETIC; RECOMBINATION, GENETIC;

BACTERIA (MICROORGANISMS); EHRLICHIA RUMINANTIUM; IXODIDA;

EID: 77956265817     PISSN: 15671348     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.meegid.2010.05.011     Document Type: Article

References (79)

1. Adakal H., Meyer D., Carasco-Lacombe C., Pinarello V., Allègre F., Huber K., Stachurski F., Morand S., Martinez D., Lefrançois T., Vachiery N., Frutos R. MLST scheme of Ehrlichia ruminantium: genomic stasis and recombination in strains from Burkina Faso. Infect. Genet. Evol. 2009, 9:1320-1328.
2. Ahmed N., Dev S.M., de Valverde M.L., Vijayachar P., Machangu R.S., Ellis W.A., Hartskeerl R.A. Multilocus sequence typing method for identification and genotypic classification of pathogenic Leptospira species. Ann. Clin. Microbiol. Antimicrob. 2006, 5:28. 10.1186/1476-0711-5.
3. Allsopp M.T.E.P., Dorfling C.M., Maillard J.C., Bensaid A., Haydon D.T., van Heerden H., Allsopp B.A. Ehrlichia ruminantium major antigenic protein gene (map1) variants are not geographically constrained and show no evidence of having evolved under positive selection pressure. J. Clin. Microbiol. 2001, 39:4200-4203.
4. Allsopp M.T., Van Heerden H., Steyn H.C., Allsopp B.A. Phylogenetic relationships among Ehrlichia ruminantium isolates. Ann. N. Y. Acad. Sci. 2003, 990:685-691.
5. Allsopp M.T.E.P., Allsopp B.A. Extensive genetic recombination occurs in the field between different genotypes of Ehrlichia ruminantium. Vet. Microbiol. 2007, 124:58-65.
6. Barre N., Uilenberg G., Morel P.C., Camus E. Danger of introducing heartwater onto the American mainland: potential role of indigenous and exotic Amblyomma ticks. Onderstepoort J. Vet. Res. 1987, 54:406-416.
7. Bekker C.P.J., Postigo M., Taoufik A., Bell-Sakyi L., Ferraz C., Martinez D., Jongejan F. Transcription analysis of the major antigenic protein 1 multigene family of three in vitro cultured Ehrlichia ruminantium isolates. J. Bacteriol. 2005, 187:4782-4791.
8. Chevenet F., Brun C., Bañuls A.L., Jacq B., Christen R. TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinf. 2006, 7:439.
9. Collins N.E., Pretorius A., Van Kleef M., Brayton K.A., Zweygarth E., Allsopp B.A. Development of improved vaccines for heartwater. Ann. N. Y. Acad. Sci. 2003, 990:474-484.
10. Collins N.E., Pretorius A., van Kleef M., Brayton K.A., Allsopp T.M., Zweygarth E., Allsopp B.A. Development of improved attenuated and nucleic acid vaccines for heartwater. Dev. Biol. 2003, 114:121-136.
11. Collins N.E., Liebenberg J., De Villiers E.P., Brayton K.A., Louw E., Pretorius A., Faber F.E., Van Heerden H., Josemans A., Van Kleef M., Steyn H.C., van Striip M.F., Zweygarth E., Jongejan F., Maillard J.C., Berthier D., Botha M., Joubert F., Corton C.H., Thomson N.R., Allsopp T.M., Allsopp B.A. The genome of the heartwater agent Ehrlichia ruminantium contains multiple tandem repeats of actively variable number. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:838-843.
12. Dame J.B., Mahan S.M., Yowell C.A. Phylogenetic relationship of Cowdria ruminantium, agent of heartwater, to Anaplasma marginale and other members of the order Rickettsiales determined on the basis of 16S rRNA sequence. Int. J. Syst. Bacteriol. 1992, 42:270-274.
13. Didelot X., Falush D. Inference of bacterial microevolution using multilocus sequence data. Genetics 2007, 175:1251-1266.
14. Du Plessis J.L. A method for determining the Cowdria ruminantium infection rate of Amblyomma hebraeum: effects in mice injected with tick homogenates. Onderstepoort J. Vet. Res. 1985, 52:55-61.
15. Du Plessis J.L., Van Gas L., Olivier J.A., Bezuidenhout J.D. The heterogenicity of Cowdria ruminantium stocks: cross-immunity and serology in sheep and pathogenicity to mice. Onderstepoort J. Vet. Res. 1989, 56:195-201.
16. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl. Acids Res. 2004, 32:1792-1797.
17. Faburay B., Jongejan F., Taoufik A., Ceesay A., Geysen D. Genetic diversity of Ehrlichia ruminantium in Amblyomma variegatum ticks and small ruminants in The Gambia determined by restriction fragment profile analysis. Vet. Microbiol. 2007, 126:189-199.
18. Fares M.A., Moya A., Barrio E. GroEL and the maintenance of bacterial endosymbiosis. Trends Genet. 2004, 20:413-416.
19. Fares M.A., Moya A., Barrio E. Adaptive evolution in GroEL from distantly related endosymbiotic bacteria of insects. J. Evol. Biol. 2005, 18:651-660.
20. Fares M.A., Travers S.A. A novel method for detecting intramolecular coevolution: adding a further dimension to selective constraints analyses. Genetics 2006, 173:9-23.
21. Fares M.A., Barrio E., Sabater-Muñoz B., Moya A. The evolution of the heat-shock protein GroEL from Buchnera, the primary endosymbiont of aphids, is governed by positive selection. Mol. Biol. Evol. 2002, 19:1162-1170.
22. Feil E.J., Li B.C., Aanensen D.M., Hanage W.P., Spratt B.G. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J. Bacteriol. 2004, 186:1518-1530.
23. Fenton W.A., Horwich A.L. GroEL-mediated protein folding. Protein Sci. 1997, 6:743-760.
24. Frutos R., Viari A., Ferraz C., Morgat A., Eychenié S., Kandassamy Y., Chantal I., Bensaid A., Coissac E., Vachiery N., Demaille J., Martinez D. Comparative genomic analysis of three strains of Ehrlichia ruminantium reveals an active process of genome size plasticity. J. Bacteriol. 2006, 188:2533-2542.
25. Frutos R., Viari A., Vachiery N., Boyer F., Martinez D. Ehrlichia ruminantium: genomic and evolutionary features. Trends Parasitol. 2007, 23:414-419.
26. Fu Y.X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 1997, 147:915-925.
27. Fu Y.X., Li W.H. Statistical tests of neutrality of mutations. Genetics 1993, 133:693-709.
28. Gething M.J., Sambrook J. Protein folding in the cell. Nature 1992, 355:33-45.
29. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
30. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids. Symp. Ser. 1999, 41:95-98.
31. Harbottle H., White D.G., McDermott P.F., Walker R.D., Zhao S. Comparison of multilocus sequence typing, pulsed-field gel electrophoresis, and antimicrobial susceptibility typing for characterization of Salmonella enterica serotype Newport isolates. J. Clin. Microbiol. 2006, 44:2449-2457.
32. Hartl F.U. Molecular chaperone in cellular protein folding. Nature 1996, 381:571-580.
33. Hey J. The structure of genealogies and the distribution of fixed differences between DNA sequence samples from natural populations. Genetics 1991, 128:831-840.
34. Hill W.G., Robertson A. Linkage disequilibrium in finite populations. Theor. Appl. Genet. 1968, 38:226-231.
35. Hughes A.L., French J.O. Homologous recombination and the pattern of nucleotide substitution in Ehrlichia ruminantium. Gene 2007, 387:31-37.
36. Inokuma H., Brouqui P., Drancourt M., Raoult D. Citrate synthase gene sequence: a new tool for phylogenetic analysis and identification of Ehrlichia. J. Clin. Microbiol. 2001, 39:3031-3039.
37. Jongejan F. Protective immunity to heartwater (Cowdria ruminantium infection) is acquired after vaccination with in vitro-attenuated Rickettsiae. Infect. Immun. 1991, 59:729-731.
38. Jukes T.H., Cantor C.R. Evolution of protein molecules. Mammalian Protein Metabolism 1969, 21-132. Academic Press, New York. H.N. Munro (Ed.).
39. Kellly J.K. A test of neutrality based on interlocus associations. Genetics 1997, 146:1197-1206.
40. Kimura M. The Neutral Theory of Molecular Evolution 1983, Cambridge University Press, Cambridge, MA, USA.
41. Klasson L., Andersson S.G.E. Evolution of minimal-gene-sets in host-dependent bacteria. Trends Microbiol. 2004, 12:37-43.
42. Librado P., Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
43. Llorca O., Galan A., Carrascosa J.L., Muga A., Valpuesta J.M. GroEL under heat-shock. Switching from a folding to a storing function. J. Biol. Chem. 1998, 273:32587-32594.
44. Lynch M., Crease T.J. The analysis of population survey data on DNA sequence variation. Mol. Biol. Evol. 1990, 7:377-394.
45. Mahan S.M., Barbet A.F., Burridge M.J. Development of improved vaccines for heartwater. Dev. Biol. 2003, 114:137-145.
46. Mahan S.M., Waghela S.D., McGuire T.C., Rurangirwa F.R., Wassink L.A., Barbet A.F. A cloned DNA probe for Cowdria ruminantium hybridizes with eight heartwater strains and detects infected sheep. J. Clin. Microbiol. 1992, 30:981-986.
47. Mahan S.M., Peter T.F., Simbi B.H., Burridge M.J. PCR detection of Cowdria ruminantium infection in ticks and animals from heartwater-endemic regions of Zimbabwe. Trop. Vet. Med. 1998, 849:85-87.
48. Martinez D., Maillard J.C., Coisne S., Sheikboudou C., Bensaid A. Protection of goats against heartwater acquired by immunisation with inactivated elementary bodies of Cowdria ruminantium. Vet. Immunol. Immunopathol. 1994, 41:153-163.
49. Martinez D., Perez J.M., Sheikboudou C., Debus A., Bensaid A. Comparative efficacy of Freund's and Montanide ISA50 adjuvants for the immunisation of goats against heartwater with inactivated Cowdria ruminantium. Vet. Parasitol. 1996, 67:175-184.
50. Martinez D., Vachiery N., Stachurski F., Kandassamy Y., Raliniaina M., Aprelon R., Gueyve A. Nested PCR for the detection and genotyping of Ehrlichia ruminantium. Use in genetic diversity analysis. Ann. N. Y. Acad. Sci. 2004, 1026:106-113.
51. McCombie R.L., Finkelstein R.A., Wood D.E. Multilocus sequence typing of historical Burkholderia pseudomallei isolates collected in Southeast Asia from 1964 to 1967 provides insight into the epidemiology of melioidosis. J. Clin. Microbiol. 2006, 44:2951-2962.
52. Molia S., Frebling M., Vachiery N., Pinarello V., Petitclerc M., Rousteau A., Martinez D., Lefrançois T. Amblyomma variegatum in cattle in Marie Galante. French Antilles: prevalence, control measures, and infection by Ehrlichia ruminantium. Vet. Parasitol. 2008, 153:338-346.
53. Moran N.A. Accelerated evolution and Muller's ratchet in endosymbiotic bacteria. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:2873-2878.
54. Moran N.A., Mira A. The process of genome shrinkage in the obligate symbiont Buchnera aphidicola. Genome Biol. 2001, 2:0054.1-0054.12.
55. Moran N.A., Plague G.R. Genomic changes following host restriction in bacteria. Curr. Opin. Genet. Dev. 2004, 14:627-633.
56. Nei M. Molecular Evolutionary Genetics 1987, Columbia University Press, New York.
57. Nei M., Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 1986, 3:418-426.
58. Perez J.-M., Martinez D., Debus A., Sheikboudou C., Bensaid A. Detection of genomic polymorphisms among isolates of the bacterium Cowdria ruminantium by random amplified polymorphic DNA and Southern blotting. FEMS Microbiol. Lett. 1997, 154:73-79.
59. Peter T.F., Deem S.L., Barbet A.F., Norval R.A., Kimby B.H., Kelly P.J., Mahan S.M. Development and evaluation of PCR assay for detection of low levels of Cowdria ruminantium infection in Amblyomma ticks not detected by DNA probe. J. Clin. Microbiol. 1995, 33:166-172.
60. Posada D. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 2008, 25:1253-1256.
61. Raliniaina M., Meyer D., Pinarello V., Sheikboudou C., Emboule L., Kandassamy Y., Adakal H., Stachurski F., Martinez D., Lefrancois T., Vachiery N. Mining the genetic diversity of Ehrlichia ruminantium using map genes family. Vet. Parasitol. 2010, 167:187-195.
62. Ranson N.A., White H.E., Saibil H.R. Chaperonins. Biochem. J. 1998, 333:233-242.
63. Reddy G., Sulsona C.R., Harrison R.H., Mahan S.M., Burridge M.J., Barbet A.F. Sequence heterogeneity of the major antigenic protein 1 genes from Cowdria ruminantium isolates from different geographical areas. Clin. Diag. Lab. Immunol. 1996, 3:417-422.
64. Sallstrom B., Andersson S.G. Genome reduction in the alpha-proteobacteria. Curr. Opin. Microbiol. 2005, 8:579-585.
65. Spratt B.G., Hanage W.P., Li B., Aanensen D.M., Feil E.J. Displaying the relatedness among isolates of bacterial species-the eBURST approach. FEMS Microbiol. Lett. 2004, 241:129-134.
66. Tajima F. Evolutionary relationship of DNA sequences in finite populations. Genetics 1983, 105:437-460.
67. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989, 123:585-595.
68. Tamas I., Klasson L., Canback B., Naslund A.K., Eriksson A.S., Wernegreen J.J., Sandstrom J.P., Moran N.A., Andersson S.G.E. 50 million years of genomic stasis in endosymbiotic bacteria. Science 2002, 296:2376-2379.
69. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 1997, 25:4876-4882.
70. Tokuriki N., Tawfik D.S. Chaperonin overexpression promotes genetic variation and enzyme evolution. Nature 2009, 459:668-673.
71. Uilenberg G., Camus E., Barre N. Some observations on a stock of Cowdria ruminantium from Guadeloupe (French West Indies). Rev. Elev. Med. Vet. Pays Trop. 1985, 34:34-42.
72. Urwin R., Maiden M.C. Multi-locus sequence typing: a tool for global epidemiology. Trends Microbiol. 2003, 11:479-487.
73. Vachiery N., Maganga G., Lefrançois T., Kandassamy Y., Stachurski F., Adakal H., Ferraz C., Morgat A., Bensaid A., Coissac E., Boyer F., Demaille J., Viari A., Martinez D., Frutos R. Differential strain-specific diagnosis of the heartwater agent: Ehrlichia ruminantium. Infect. Genet. Evol. 2008, 8:459-466.
74. van Vliet A.H.M., Jongejan F., van Der Zeijst B.A.M. Phylogenetic position of Cowdria ruminantium (Rickettsiales) determined by analysis of amplified 16S ribosomal DNA sequences. Int. J. Syst. Bacteriol. 1992, 42:494-498.
75. Van Vliet A.H., van der Zeijst B.A., Camus E., Mahan S.M., Martinez D., Jongejan F. Use of a specific immunogenic region on the Cowdria ruminantium MAP1 protein in a serological assay. J. Clin. Microbiol. 1995, 33:2405-2410.
76. Waghela S.D., Rurangirwa F.R., Mahan S.M., Yunker C.E., Crawford T.B., Barbet A.F., Burridge M.J., McGuire T.C. A cloned DNA probe identifies Cowdria ruminantium in Amblyomma variegatum ticks. J. Clin. Microbiol. 1991, 29:2571-2577.
77. Wall J.D. Recombination and the power of statistical tests of neutrality. Genet. Res. 1999, 74:65-69.
78. Watterson G.A. On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 1975, 7:256-276.
79. Zweygarth E., Josemans A.I., Van Strijp M.F., Lopez-Rebollar L., Van Kleef M., Allsopp B.A. An attenuated Ehrlichia ruminantium (Welgevonden stock) vaccine protects small ruminants against virulent heartwater challenge. Vaccine 2005, 23:1695-1702.