Comparative genomic analysis of three strains of Ehrlichia ruminantium reveals an active process of genome size plasticity

Journal of Bacteriology

Volumn 188, Issue 7, 2006, Pages 2533-2542

  Frutos, Roger ^a   Viari, Alain ^b   Ferraz, Conchita ^c   Morgat, Anne ^b,d   Eychenié, Sophie ^c   Kandassamy, Yane ^a   Chantal, Isabelle ^a   Bensaid, Albert ^a,e   Coissac, Eric ^b   Vachiery, Nathalie ^a   Demaille, Jacques ^c   Martinez, Dominique ^a  

^a CIRAD   (France)

^b INRIA RHÔNE ALPES   (France)

^c INSTITUTE OF HUMAN GENETICS   (France)

^d SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^e CENTRE DE RECERCA EN SANITAT ANIMAL CRESA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA;

AFRICA; ANAPLASMA; ARTICLE; CARIBBEAN ISLANDS; COMPARATIVE GENE MAPPING; EHRLICHIA RUMINANTIUM; GENE SEQUENCE; GENETIC CONSERVATION; GENOME SIZE; HEARTWATER DISEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PHENOTYPE; PRIORITY JOURNAL; RICKETTSIA; RICKETTSIALES; STRAIN DIFFERENCE; STRUCTURAL GENOMICS; TANDEM REPEAT; TICK BORNE DISEASE; TUF GENE; WOLBACHIA;

ACARI; ANAPLASMA; ANAPLASMA MARGINALE; BACTERIA (MICROORGANISMS); EHRLICHIA RUMINANTIUM; RICKETTSIA; RICKETTSIACEAE; RICKETTSIALES; WOLBACHIA;

EID: 33645285639     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.188.7.2533-2542.2006     Document Type: Article

References (71)

1. Abdulkarim, F., and D. Hughes. 1996. Homologous recombination between the tuf genes of Salmonella typhimurium. J. Mol. Biol. 260:506-522.
2. Achaz, G., P. Netter, and E. Coissac. 2001. Study of intrachromosomal duplications among the eukaryote genomes. Mol. Biol. Evol. 18:2280-2288.
3. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
4. Amiri, H., C. M. Alsmark, and S. G. E. Andersson. 2002. Proliferation and deterioration of Rickettsia palindromic elements. Mol. Biol. Evol. 19:1234-1243.
5. Amiri, H., W. Davids, and S. G. E. Andersson. 2003. Birth and death of orphan genes in Rickettsia. Mol. Biol. Evol. 20:1575-1587.
6. Andersson, S. G., and C. G. Kurland. 1998. Reductive evolution of resident genomes. Trends Microbiol. 6:263-268.
7. Andersson, S. G., A. Zomorodipour, J. O. Andersson, T. Sicheritz-Ponten, U. C. Alsmark, R. M. Podowski, A. K. Naslund, A. S. Eriksson, H. H. Winkler, and C. G. Kurland. 1998. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133-140.
8. Barré, N., G. Uilenberg, P. C. Morel, and E. Camus. 1987. Danger of introducing heartwater onto the American mainland: potential role of indigenous and exotic Amblyomma ticks. Onderstepoort J. Vet. Res. 54:406-416.
9. Bekker, C. P. J., M. Postigo, A. Taoufik, L. Bell-Sakyi, C. Ferraz, D. Martinez, and F. Jongejan. 2005. Transcription analysis of the major antigenic protein 1 multigene family of three in vitro cultured Ehrlichia ruminantium isolates. J. Bacteriol. 187:4782-4791.
10. Benson, G. 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 57:573-580.
11. Berg, O. G., and C. G. Kurland. 2002. Evolution of microbial genomes: sequence acquisition and loss. Mol. Biol. Evol. 19:2265-2276.
12. Bezuidenhout, J. D. 1989. Cowdria vaccines, p. 31-42. In I. G. Wright (ed.), Veterinary protozoan and hemoparasite vaccines. CRC Press, Inc., Boca Raton, Fla.
13. Bezuidenhout, J. D., C. L. Paterson, and B. J. Barnard. 1985. In vitro cultivation of Cowdria ruminantium. Onderstepoort J. Vet. Res. 52:113-120.
14. Boeckmann, B., A. Bairoch, R. Apweiler, M. C. Blatter, A. Estreicher, E. Gasteiger, M. J. Martin, K. Michoud, C. O'Donovan, I. Phan, S. Pilbout, and M. Schneider. 2003. The SWISS-PROT protein knowledge base and its supplement TrEMBL in 2003. Nucleic Acids Res. 31:365-370.
15. Borodovsky, M., and J. McIninch. 1993. GENEMARK: parallel recognition for both DNA strands. Comput. Chem. 17:123-133.
16. Brayton, K. A., L. S. Kappmeyer, D. R. Herndon, M. J. Dark, D. L. Tibbals, G. H. Palmer, T. C. McGuire, and D. P. Knowles, Jr. 2005. Complete genome sequencing of Anaplasma marginale reveals that the surface is skewed to two superfamilies of outer membrane proteins. Proc. Natl. Acad. Sci. USA 102:844-849.
17. Burridge, M. J. J., L. A. Simmons, T. F. Peter, and S. M. Mahan. 2002. Increasing risks of introduction of heartwater onto the American mainland associated with animal movements. Ann. N. Y. Acad. Sci. 969:269-274.
18. Bzymek, M., and S. T. Lovett. 2001. Instability of repetitive DNA sequences: the role of replication in multiple mechanisms. Proc. Natl. Acad. Sci. USA 98:8319-8325.
19. Cole, S. T., K. Eiglmeier, J. Parkhill, K. D. James, N. R. Thomson, P. R. Wheeler, N. Honore, T. Garnier, C. Churcher, D. Harris, K. Mungall, D. Basham, D. Brown, T. Chillingworth, R. Connor, R. M. Davies, K. Devlin, S. Duthoy, T. Feltwell, A. Fraser, N. Hamlin, S. Holroyd, T. Hornsby, K. Jagels, C. Lacroix, J. Maclean, S. Moule, L. Murphy, K. Oliver, M. A. Quail, M. A. Rajandream, K. M. Rutherford, S. Rutter, K. Seeger, S. Simon, M. Simmonds, J. Skelton, R. Squares, S. Squares, K. Stevens, K. Taylor, S. Whitehead, J. R. Woodward, and B. G. Barrell. 2001. Massive gene decay in the leprosy bacillus. Nature 409:1007-1111.
20. Collins, N. E., A. Pretorius, M. Van Kleef, K. A. Brayton, E. Zweygarth, and B. A. Allsopp. 2003. Development of improved vaccines for heartwater. Ann. N. Y. Acad. Sci. 990:474-484.
21. Collins, N. E., E. P. De Villiers, K. A. Brayton, and B. A. Allsopp. 1998. DNA sequence of a cosmid clone of Cowdria ruminantium. Dev. Biol. 114:365-368.
22. Collins, N. E., J. Liebenberg, E. P. De Villiers, K. A. Brayton, E. Louw, A. Pretorias, F. E. Faber, H. Van Heerden, A. Josemans, M. Van Kleef, H. C. Steyn, M. F. van Strijp, E. Zweygarth, F. Jongejan, J. C. Maillard, D. Berthier, M. Botha, F. Joubert, C. H. Corton, N. R. Thomson, M. T. Allsopp, and B. A. Allsopp. 2005. The genome of the heartwater agent Ehrlichia ruminantium contains multiple tandem repeats of actively variable number. Proc. Natl. Acad. Sci. USA 102:838-843.
23. Dumler, J. S., A. F. Barbet, C. P. Bekker, G. A. Dasch, G. H. Palmer, S. C. Ray, Y. Rikihisa, and F. R. Rurangirwa. 2001. 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. 51:2145-2165.
24. Du Plessis, J. L. 1985. A method for determining the Cowdria ruminantium infection rate of Amblyomma hebraeum: effects in mice injected with tick homogenates. Onderstepoort J. Vet. Res. 52:55-61.
25. Durand, P., C. Medigue, A. Morgat, Y. Vandenbrouck, A. Viari, and F. Rechenmann. 2003. Integration of data and methods for genome analysis. Curr. Opin. Drug Discov. Devel. 6:346-352.
26. Fenollar, F., B. La Scola, H. Inokuma, J. S. Dumler, M. J. Taylor, and D. Raoult. 2003. Culture and phenotypic characterization of a Wolbachia pipientis isolate. J. Clin. Microbiol. 41:5434-5441.
27. Foster, J., M. Ganatra, I. Kamal, J. Ware, K. Makarova, N. Ivanova, A. Bhattacharyya, V. Kapatral, S. Kumar, J. Posfai, T. Vincze, J. Ingram, L. Moran, A. Lapidus, M. Omelchenko, N. Kyrpides, E. Ghedin, S. Wang, E. Goltsman, V. Joukov, O. Ostrovskaya, K. Tsukerman, M. Mazur, D. Comb, E. Koonin, and B. Slatko. 2005. The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol. 3:599-614.
28. Grigoriev, A. 1998. Analyzing genomes with cumulative skew diagrams. Nucleic Acids Res. 26:2286-2290.
29. Harrison, P. M., and M. Gerstein. 2002. Studying genomes through the aeons: protein families, pseudogenes and proteome evolution. J. Mol. Biol. 318:1155-1174.
30. Hong, G., E. C. Yao-Yu, Z. Shuping, T. Min, T. Mong-Hsun, J. T. Joseph, L. R. Allen, and C. Wei-Mei. 2004. Comparative genomics of Rickettsia prowazekii Madrid E and Breinl strains. J. Bacteriol. 186:556-565.
31. Horn, M., A. Collingro, S. Schmitz-Esser, C. L. Beier, U. Purkhold, B. Fartmann, P. Brandt, G. J. Nyakatura, M. Droege, D. Frishman, T. Rattei, H. W. Mewes, and M. Wagner. 2004. Illuminating the evolutionary history of Chlamydiae. Science 304:728-730.
32. Hughes, D. 2000. Co-evolution of the tuf genes links gene conversion with the generation of chromosomal inversions. J. Mol. Biol. 297:355-364.
33. Jongejan, F. 1991. Protective immunity to heartwater (Cowdria ruminantium infection) is acquired after vaccination with in vitro-attenuated rickettsiae. Infect. Immun. 59:729-731.
34. Jongejan, F., N. De Vries, J. Nieuwenhuijs, L. A. Wassink, and A. H. M. Van Vliet. 1993. The immunodominant 32-kilodalton protein of Cowdria ruminantium is conserved within the genus Ehrlichia. Rev. Elev. Med. Vet. Trop. 46:145-152.
35. Karlin, S., G. Ghandour, F. Ost, S. Tavare, and L. J. Korn. 1983. New approaches for computer analysis of nucleic acid sequences. Proc. Natl. Acad. Sci. USA 80:5660-5664.
36. Katz, J. B., R. DeWald, J. E. Dawson, E. Camus, D. Martinez, and R. Mondry. 1997. Development and evaluation of a recombinant antigen, monoclonal antibody-based competitive ELISA for heartwater serodiagnosis. J. Vet. Diagn. Investig. 9:130-135.
37. Klasson, L., and S. G. E. Andersson. 2004. Evolution of minimal-gene-sets in host-dependent bacteria. Trends Microbiol. 12:37-43.
38. Lovett, S. T. 2004. Encoded errors: mutations and rearrangements mediated by misalignment at repetitive DNA sequences. Mol. Microbiol. 52:1243-1253.
39. Martinez, D., N. Vachiery, F. Stachurski, Y. Kandassamy, M. Raliniaina, R. Aprelon, and A. Gueye. 2005. Nested PCR for the detection and genotyping of Ehrlichia ruminantium. Use in genetic diversity analysis. Ann. N. Y. Acad. Sci. 1026:106-113.
40. Martinez, D., J. C. Maillard, S. Coisne, C. Sheikboudou, and A. Bensaid. 1994. Protection of goats against heartwater acquired by immunisation with inactivated elementary bodies of Cowdria ruminantium. Vet. Immunol. Immunopathol. 41:153-163.
41. Martinez, D., J. Swinkels, E. Camus, and F. Jongejan. 1990. Comparison between 3 antigens for the serodiagnosis of heartwater disease by indirect immunofluorescence. Rev. Elev. Med. Vet. Pays Trop. 43:159-166.
42. McLeod, M. P., X. Qin, S. E. Karpathy, J. Gioia, S. K. Highlander, G. E. Fox, T. Z. McNeill, H. Jiang, D. Muzny, L. S. Jacob, A. C. Hawes, E. Sodergren, R. Gill, J. Hume, M. Morgan, G. Fan, A. G. Amin, R. A. Gibbs, C. Hong, X. J. Yu, D. H. Walker, and G. M. Weinstock. 2004. Complete genome sequence of Rickettsia typhi and comparison with sequences of other rickettsiae. J. Bacteriol. 186:5842-5855.
43. Mira, A., H. Ochman, and N. A. Moran. 2001. Deletional bias and the evolution of bacterial genomes. Trends Genet. 17:589-596.
44. Mira, A., L. Klasson, and S. G. E. Andersson. 2002. Microbial genome evolution: sources of variability. Curr. Opin. Microbiol. 5:506-512.
45. Mondry, R., D. Martinez, E. Camus, A. Liebisch, J. B. Katz, R. Dewald, A. H. van Vliet, and F. Jongejan. 1998. Validation and comparison of three enzyme-linked immunosorbent assays for the detection of antibodies to Cowdria ruminantium infection. Ann. N. Y. Acad. Sci. 849:262-272.
46. Moran, N. A., and A. Mira. 2001. The process of genome shrinkage in the obligate symbiont Buchnera aphidicola. Genome Biol. 2:RESEARCH0054.1-0054.12. [Online.] http://genomebiology.eom/2001/2/12/RESEARCH/0054.
47. Moran, N. A., and G. R. Plague. 2004. Genomic changes following host restriction in bacteria. Curr. Opin. Genet. Dev. 14:627-633.
48. Mukhebi, A. W., T. Chamboko, C. J. O'Callaghan, T. F. Peter, R. L. Kruska, G. F. Medley, S. M. Mahan, and B. D. Perry. 1999. An assessment of the economic impact of heartwater (Cowdria ruminantium infection) and its control in Zimbabwe. Prev. Vet. Med. 39:173-189.
49. Nei, M., and T. Gojobori. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3:418-426.
50. Ogata, H., S. Audic, P. Renesto-Audiffren, P. E. Fournier, V. Barbe, D. Samson, V. Roux, P. Cossart, J. Weissenbach, J. M. Claverie, and D. Raoult. 2001. Mechanisms of evolution in Rickettsia conorii and R. prowazekii. Science 293:2093-2098.
51. Ohashi, N., N. Zhi, Q. Lin, and Y. Rikihisa. 2002. Characterization and transcriptional analysis of gene clusters for a type IV secretion machinery in human granulocytic and monocytic ehrlichiosis agents. Infect. Immun. 70: 2128-2138.
52. Pascal, G., C. Medigue, and A. Danchin. 2005. Universal biases in protein composition of model prokaryotes. Proteins 60:27-35.
53. Pegram, R. P., E. F. Gersabeck, D. Wilson, and J. W. Hansen. 2002. Eradication of the tropical bont tick in the Caribbean: is the Caribbean Amblyomma Program in a crisis? Ann. N. Y. Acad. Sci. 969:297-305.
54. Perez, J. M., D. Martinez, A. Debus, C. Sheikboudou, and A. Bensaid. 1997. Detection of genomic polymorphisms among isolates of the intracellular bacterium Cowdria ruminantium by random amplified polymorphic DNA and Southern blotting. FEMS Microbiol. Lett. 154:73-79.
55. Perriere, G., and J. Thioulouse. 2003. Use of correspondence discriminant analysis to predict the subcellular location of bacterial proteins. Comput. Methods Programs Biomed. 70:99-110.
56. Provost, A., and J. D. Bezuidenhout. 1987. The historical background and global importance of heartwater. Onderstepoort J. Vet. Res. 54:165-169.
57. Rocha, E. P. C., A. Danchin, and A. Viari. 1999. Universal replication biases in bacteria. Mol. Microbiol. 32:11-16.
58. Stepkowski, T., and B. Legocki. 2001. Reduction of bacterial genome size and expansion resulting from obligate intracellular lifestyle and adaptation to soil habitat. Acta Biochim. Pol. 48:367-381.
59. Syvanen, A. C., H. Amiri, A. Jamal, S. G. Andersson, and C. G. Kurland. 1996. A chimeric disposition of the elongation factor genes in Rickettsia prowazekii. J. Bacteriol. 178:6192-6199.
60. Taillardat-Bisch, A. V., D. Raoult, and M. Drancourt. 2003. RNA polymerase beta-subunit-based phylogeny of Ehrlichia spp., Anaplasma spp., Neorickettsia spp. and Wolbachia pipientis. Int. J. Syst. Evol. Microbiol. 53:455-458.
61. Tamas, I., L. Klasson, B. Canback, A. K. Naslund, A. S. Eriksson, J. J. Wernegreen, J. P. Sandstrom, N. A. Moran, and S. G. E. Andersson. 2002. 50 million years of genomic stasis in endosymbiotic bacteria. Science 296: 2376-2379.
62. Tatusov, R. L., N. D. Fedorova, J. D. Jackson, A. R. Jacobs, B. Kiryutin, E. V. Koonin, D. M. Krylov, R. Mazumder, S. L. Mekhedov, A. N. Nikolskaya, B. S. Rao, S. Smirnov, A. V. Sverdlov, S. Vasudevan, Y. I. Wolf, J. J. Yin, and D. A. Natale. 2003. The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:41-54.
63. Tatusov, R. L., E. V. Koonin, and D. J. Lipman. 1997. A genomic perspective on protein families. Science 278:631-637.
64. Uilenberg, G., E. Camus, and N. Barré. 1985. Some observations on a stock of Cowdria ruminantium from Guadeloupe (French West Indies). Rev. Elev. Med. Vet. Pays Trop. 34:34-42.
65. Van Vliet, A. H., B. A. van der Zeyst, E. Camus, S. M. Mahan, D. Martinez, and F. Jongejan. 1995. Use of a specific immunogenic region on the Cowdria ruminantium MAP1 protein in a serological assay. J. Clin. Microbiol. 33: 2405-2410.
66. Weisburg, W. G., S. M. Barns, D. A. Pelletier, and D. J. Lane. 1991. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173:697-703.
67. Wu, M., L. V. Sun, J. J. Vamathevan, M. Riegler, R. T. DeBoy, J. C. Brownlie, E. A. McGraw, W. Martin, C. Esser, N. Ahmadinejad, C. Wiegand, R. Madupu, M. J. Beanan, L. M. Brinkac, S. C. Daugherty, A. S. Durkin, J. F. Kolonay, W. C. Nelson, Y. Mohamoud, P. Lee, K. Berry, M. B. Young, T. Utterback, J. Weidman, W. C. Nierman, I. T. Paulsen, K. E. Nelson, H. Tettelin, S. L. O'Neill, and J. A. Eisen. 2004. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol. 2:327-341.
68. Wuyts, J., G. Perrière, and Y. Van de Peer. 2004. The European ribosomal RNA database. Nucleic Acids Res. 32:D101-D103.
69. Zhang, J., S. Kumar, and M. Nei. 1997. Small-sample tests of episodic adaptive evolution: a case study of primate lysozymes. Mol. Biol. Evol. 14:1335-1338.
70. Zomorodipour, A., and S. G. Andersson. 1999. Obligate intracellular parasites: Rickettsia prowazekii and Chlamydia trachomatis. FEBS Lett. 452:11-15.
71. Zweygarth, E., A. I. Josemans, M. F. Van Strijp, L. Lopez-Rebollar, M. Van Kleef, and B. A. Allsopp. 2005. An attenuated Ehrlichia ruminantium (Welgevonden stock) vaccine protects small ruminants against virulent heartwater challenge. Vaccine 23:1695-1702.