Genome sequence of the deep-rooted Yersinia pestis strain angola reveals new insights into the evolution and pangenome of the plague bacterium

Journal of Bacteriology

Volumn 192, Issue 6, 2010, Pages 1685-1699

  Eppinger, Mark ^a   Worsham, Patricia L ^b   Nikolich, Mikeljon P ^c   Riley, David R ^a   Sebastian, Yinong ^d   Mou, Sherry ^b   Achtman, Mark ^e   Lindler, Luther E ^f   Ravel, Jacques ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

^c WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^d J CRAIG VENTER INSTITUTE   (United States)

^e UNIVERSITY COLLEGE CORK   (Ireland)

^f Global Emerging Infections Surveillance and Response System   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGOLA; ANIMAL EXPERIMENT; ARTICLE; BIOTYPE; CHROMOSOME; CONTROLLED STUDY; FUNGAL STRAIN; GENE IDENTIFICATION; GENE SEQUENCE; GENOME; ISOLATION PROCEDURE; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYLOGENY; PLASMID; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; VIRULENCE; YERSINIA PESTIS;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BASE SEQUENCE; EVOLUTION; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; GENOTYPE; GUINEA PIGS; MICE; MICE, INBRED BALB C; PLAGUE; PLASMIDS; VIRULENCE; WORLD HEALTH; YERSINIA PESTIS;

BACTERIA (MICROORGANISMS); YERSINIA PESTIS; YERSINIA PESTIS ANGOLA; YERSINIA PSEUDOTUBERCULOSIS;

EID: 77949412186     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01518-09     Document Type: Article

References (74)

1. Achtman, M., G. Morelli, P. Zhu, T. Wirth, I. Diehl, B. Kusecek, A. J. Vogler, D. M. Wagner, C. J. Allender, W. R. Easterday, V. Chenal-Francisque, P. Worsham, N. R. Thomson, J. Parkhill, L. E. Lindler, E. Carniel, and P. Keim. 2004. Microevolution and history of the plague bacillus, Yersinia pestis. Proc. Natl. Acad. Sci. USA 101:17837-17842.
2. Achtman, M., K. Zurth, G. Morelli, G. Torrea, A. Guiyoule, and E. Carniel. 1999. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. USA 96:14043-14048.
3. Adair, D. M., P. L. Worsham, K. K. Hill, A. M. Klevytska, P. J. Jackson, A. M. Friedlander, and P. Keim. 2000. Diversity in a variable-number tandem repeat from Yersinia pestis. J. Clin. Microbiol. 38:1516-1519.
4. Adamovicz, J. L., and P. L. Worsham. 2006. Plague, p. 107-135. In J. R. Swearengen (ed.), Biodefense: research methodology and animal models. CRC Press Taylor & Francis Group, Boca Raton, FL.
5. 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.
6. Anderson, G. W., Jr., S. E. Leary, E. D. Williamson, R. W. Titball, S. L. Welkos, P. L. Worsham, and A. M. Friedlander. 1996. Recombinant V antigen protects mice against pneumonic and bubonic plague caused by F1-capsule-positive and -negative strains of Yersinia pestis. Infect. Immun. 64:4580-4585.
7. Anisimov, A. P., L. E. Lindler, and G. B. Pier. 2004. Intraspecific diversity of Yersinia pestis. Clin. Microbiol. Rev. 17:434-464.
8. Auerbach, R. K., A. Tuanyok, W. S. Probert, L. Kenefic, A. J. Vogler, D. C. Bruce, C. Munk, T. S. Brettin, M. Eppinger, J. Ravel, D. M. Wagner, and P. Keim. 2007. Yersinia pestis evolution on a small timescale: comparison of whole genome sequences from North America. PLoS One 2:e770.
9. Bearden, S. W., C. Sexton, J. Pare, J. M. Fowler, C. G. Arvidson, L. Yerman, R. E. Viola, and R. R. Brubaker. 2009. Attenuated enzootic (pestoides) isolates of Yersinia pestis express active aspartase. Microbiology 155:198-209.
10. Burrows, T. W. 1957. Virulence of Pasteurella pestis. Nature 179:1246-1247.
11. Carniel, E., and B. J. Hinnebusch (ed.). 2004. Yersinia molecular and cellular biology. Horizon Biosciences, Norfolk NR18 0JA, United Kingdom.
12. Chain, P. S., E. Carniel, F. W. Larimer, J. Lamerdin, P. O. Stoutland, W. M. Regala, A. M. Georgescu, L. M. Vergez, M. L. Land, V. L. Motin, R. R. Brubaker, J. Fowler, J. Hinnebusch, M. Marceau, C. Medigue, M. Simonet, V. Chenal-Francisque, B. Souza, D. Dacheux, J. M. Elliott, A. Derbise, L. J. Hauser, and E. Garcia. 2004. Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. USA 101:13826-13831.
13. Chain, P. S. G., P. Hu, S. A. Malfatti, L. Radnedge, F. Larimer, L. M. Vergez, P. Worsham, M. C. Chu, and G. L. Andersen. 2006. Complete genome sequence of Yersinia pestis strains Antiqua and Nepal516: evidence of gene reduction in an emerging pathogen. J. Bacteriol. 188:4453-4463.
14. Chu, M. C., X. Q. Dong, X. Zhou, and C. F. Garon. 1998. A cryptic 19-kilobase plasmid associated with U.S. isolates of Yersinia pestis: a dimer of the 9.5-kilobase plasmid. Am. J. Trop. Med. Hyg. 59:679-686.
15. Cornelius, C. A., L. E. Quenee, D. Elli, N. A. Ciletti, and O. Schneewind. 2009. Yersinia pestis IS1541 transposition provides for escape from plague immunity. Infect. Immun. 77:1807-1816.
16. Cummings, C. A., M. M. Brinig, P. W. Lepp, S. van de Pas, and D. A. Relman. 2004. Bordetella species are distinguished by patterns of substantial gene loss and host adaptation. J. Bacteriol. 186:1484-1492.
17. Darling, A. E., I. Miklos, and M. A. Ragan. 2008. Dynamics of genome rearrangement in bacterial populations. PLoS Genet. 4:e1000128.
18. Davis, K. J., D. L. Fritz, M. L. Pitt, S. L. Welkos, P. L. Worsham, and A. M. Friedlander. 1996. Pathology of experimental pneumonic plague produced by fraction 1-positive and fraction 1-negative Yersinia pestis in African green monkeys (Cercopithecus aethiops). Arch. Pathol. Lab. Med. 120:156-163.
19. Delcher, A. L., A. Phillippy, J. Carlton, and S. L. Salzberg. 2002. Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res. 30:2478-2483.
20. Deng, W., V. Burland, G. Plunkett, 3rd, A. Boutin, G. F. Mayhew, P. Liss, N. T. Perna, D. J. Rose, B. Mau, S. Zhou, D. C. Schwartz, J. D. Fetherston, L. E. Lindler, R. R. Brubaker, G. V. Plano, S. C. Straley, K. A. McDonough, M. L. Nilles, J. S. Matson, F. R. Blattner, and R. D. Perry. 2002. Genome sequence of Yersinia pestis KIM. J. Bacteriol. 184:4601- 4611.
21. Devignat, R. 1953. Geographical distribution of three species of Pasteurella pestis. Schweiz. Z Pathol. Bakteriol. 16:509-514.
22. Eppinger, M., Z. Guo, Y. Sebastian, Y. Song, L. E. Lindler, R. Yang, and J. Ravel. 2009. Draft genome sequences of Yersinia pestis isolates from natural foci of endemic plague in China. J. Bacteriol. 191:7628-7629.
23. Eppinger, M., M. J. Rosovitz, W. F. Fricke, D. A. Rasko, G. Kokorina, C. Fayolle, L. E. Lindler, E. Carniel, and J. Ravel. 2007. The complete genome sequence of Yersinia pseudotuberculosis IP31758, the causative agent of Far East scarlet-like fever. PLoS Genet. 3:e142.
24. Ewing, B., L. Hillier, M. C. Wendl, and P. Green. 1998. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8:175-185.
25. Filippov, A. A., N. S. Solodovnikov, L. M. Kookleva, and O. A. Protsenko. 1990. Plasmid content in Yersinia pestis strains of different origin. FEMS Microbiol. Lett. 55:45-48.
26. Friedlander, A. M., S. L. Welkos, P. L. Worsham, G. P. Andrews, D. G. Heath, G. W. Anderson, Jr., M. L. Pitt, J. Estep, and K. Davis. 1995. Relationship between virulence and immunity as revealed in recent studies of the F1 capsule of Yersinia pestis. Clin. Infect. Dis. 21(Suppl. 2):S178-S181.
27. Galimand, M., A. Guiyoule, G. Gerbaud, B. Rasoamanana, S. Chanteau, E. Carniel, and P. Courvalin. 1997. Multidrug resistance in Yersinia pestis mediated by a transferable plasmid. N. Engl. J. Med. 337:677-680.
28. Garcia, E., P. Worsham, S. Bearden, S. Malfatti, D. Lang, F. Larimer, L. Lindler, and P. Chain. 2007. Pestoides F, an atypical Yersinia pestis strain from the former Soviet Union. Adv. Exp. Med. Biol. 603:17-22.
29. Golubov, A., H. Neubauer, C. Nolting, J. Heesemann, and A. Rakin. 2004. Structural organization of the pFra virulence-associated plasmid of rhamnose-positive Yersinia pestis. Infect. Immun. 72:5613-5621.
30. Gonzalez, M. D., C. A. Lichtensteiger, R. Caughlan, and E. R. Vimr. 2002. Conserved filamentous prophage in Escherichia coli O18:K1:H7 and Yersinia pestis biovar orientalis. J. Bacteriol. 184:6050-6055.
31. Guindon, S., F. Lethiec, P. Duroux, and O. Gascuel. 2005. PHYML Online - a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res. 33:W557-W559.
32. Guiyoule, A., F. Grimont, I. Iteman, P. A. Grimont, M. Lefevre, and E. Carniel. 1994. Plague pandemics investigated by ribotyping of Yersinia pestis strains. J. Clin. Microbiol. 32:634-641.
33. Guyton, A. C. 1947. Measurement of the respiratory volumes of laboratory animals. Am. J. Physiol. 150:70.
34. Hacker, J., B. Hochhut, B. Middendorf, G. Schneider, C. Buchrieser, G. Gottschalk, and U. Dobrindt. 2004. Pathogenomics of mobile genetic elements of toxigenic bacteria. Int. J. Med. Microbiol. 293:453-461.
35. Haiko, J., M. Kukkonen, J. J. Ravantti, B. Westerlund-Wikstrom, and T. K. Korhonen. 2009. The single substitution I259T conserved in the plasminogen activator Pla of pandemic Yersinia pestis branches enhances fibrinolytic activity. J. Bacteriol. 191:4758-4766.
36. Hasegawa, M., H. Kishino, and T. Yano. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22:160-174.
37. Holden, M. T., Z. Heather, R. Paillot, K. F. Steward, K. Webb, F. Ainslie, T. Jourdan, N. C. Bason, N. E. Holroyd, K. Mungall, M. A. Quail, M. Sanders, M. Simmonds, D. Willey, K. Brooks, D. M. Aanensen, B. G. Spratt, K. A. Jolley, M. C. Maiden, M. Kehoe, N. Chanter, S. D. Bentley, C. Robinson, D. J. Maskell, J. Parkhill, and A. S. Waller. 2009. Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens. PLoS Pathog. 5:e1000346.
38. Huson, D. H., and D. Bryant. 2006. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23:254-267.
39. Huson, D. H., K. Reinert, S. A. Kravitz, K. A. Remington, A. L. Delcher, I. M. Dew, M. Flanigan, A. L. Halpern, Z. Lai, C. M. Mobarry, G. G. Sutton, and E. W. Myers. 2001. Design of a compartmentalized shotgun assembler for the human genome. Bioinformatics 17(Suppl. 1):S132-S139.
40. Jaccard, P. 1908. Nouvelles recherches sur la distribution florale. Bull. Soc. Vaudoise Sci. Nat. 44:223-270.
41. Knight, S. D. 2007. Structure and assembly of Yersinia pestis F1 antigen. Adv. Exp. Med. Biol. 603:74-87.
42. Kukleva, L. M., G. A. Eroshenko, V. E. Kuklev, N. Shavina, M. Krasnov Ia, N. P. Guseva, and V. V. Kutyrev. 2008. A study of the nucleotide sequence variability of rha locus genes of Yersinia pestis main and non-main subspecies. Mol. Gen. Mikrobiol. Virusol. 2008:23-27.
43. Kurtz, S., A. Phillippy, A. L. Delcher, M. Smoot, M. Shumway, C. Antonescu, and S. L. Salzberg. 2004. Versatile and open software for comparing large genomes. Genome Biol. 5:R12.
44. Lathem, W. W., P. A. Price, V. L. Miller, and W. E. Goldman. 2007. A plasminogen-activating protease specifically controls the development of primary pneumonic plague. Science 315:509-513.
45. Leal-Balbino, T. C., N. C. Leal, C. V. Lopes, and A. M. Almeida. 2004. Differences in the stability of the plasmids of Yersinia pestis cultures in vitro: impact on virulence. Mem. Inst. Oswaldo Cruz 99:727-732.
46. Li, Y., Y. Cui, Y. Hauck, M. E. Platonov, E. Dai, Y. Song, Z. Guo, C. Pourcel, S. V. Dentovskaya, A. P. Anisimov, R. Yang, and G. Vergnaud. 2009. Genotyping and phylogenetic analysis of Yersinia pestis by MLVA: insights into the worldwide expansion of Central Asia plague foci. PLoS One 4:e6000.
47. Li, Y., E. Dai, Y. Cui, M. Li, Y. Zhang, M. Wu, D. Zhou, Z. Guo, X. Dai, B. Cui, Z. Qi, Z. Wang, H. Wang, X. Dong, Z. Song, J. Zhai, Y. Song, and R. Yang. 2008. Different region analysis for genotyping Yersinia pestis isolates from China. PLoS One 3:e2166.
48. Medini, D., C. Donati, H. Tettelin, V. Masignani, and R. Rappuoli. 2005. The microbial pan-genome. Curr. Opin. Genet. Dev. 15:589-594.
49. Mollaret, H. H., and C. Mollaret. 1965. Melibiose fermentation in the genus Yersina and its importance in the diagnosis of the varieties of Y. pestis. Bull. Soc. Pathol. Exot. Filiales 58:154-156.
50. Motin, V. L., A. M. Georgescu, J. M. Elliott, P. Hu, P. L. Worsham, L. L. Ott, T. R. Slezak, B. A. Sokhansanj, W. M. Regala, R. R. Brubaker, and E. Garcia. 2002. Genetic variability of Yersinia pestis isolates as predicted by PCR-based IS100 genotyping and analysis of structural genes encoding glycerol-3-phosphate dehydrogenase (glpD). J. Bacteriol. 184:1019-1027.
51. Nagamatsu, T., H. Yamasaki, T. Hirota, M. Yamato, Y. Kido, M. Shibata, and F. Yoneda. 1993. Syntheses of 3-substituted 1-methyl-6- phenylpyrimido[5,4-e]-1,2,4-triazine-5,7(1H,6H)-diones (6-phenyl analogs of toxoflavin) and their 4-oxides, and evaluation of antimicrobial activity of toxoflavins and their analogs. Chem. Pharm. Bull. (Tokyo) 41:362-368.
52. Nelson, K. E., R. A. Clayton, S. R. Gill, M. L. Gwinn, R. J. Dodson, D. H. Haft, E. K. Hickey, J. D. Peterson, W. C. Nelson, K. A. Ketchum, L. McDonald, T. R. Utterback, J. A. Malek, K. D. Linher, M. M. Garrett, A. M. Stewart, M. D. Cotton, M. S. Pratt, C. A. Phillips, D. Richardson, J. Heidelberg, G. G. Sutton, R. D. Fleischmann, J. A. Eisen, O. White, S. L. Salzberg, H. O. Smith, J. C. Venter, and C. M. Fraser. 1999. Evidence for lateral gene transfer between Archaea and bacteria from genome sequence of Thermotoga maritima. Nature 399:323-329.
53. Parkhill, J., G. Dougan, K. D. James, N. R. Thomson, D. Pickard, J. Wain, C. Churcher, K. L. Mungall, S. D. Bentley, M. T. Holden, M. Sebaihia, S. Baker, D. Basham, K. Brooks, T. Chillingworth, P. Connerton, A. Cronin, P. Davis, R. M. Davies, L. Dowd, N. White, J. Farrar, T. Feltwell, N. Hamlin, A. Haque, T. T. Hien, S. Holroyd, K. Jagels, A. Krogh, T. S. Larsen, S. Leather, S. Moule, P. O'Gaora, C. Parry, M. Quail, K. Rutherford, M. Simmonds, J. Skelton, K. Stevens, S. Whitehead, and B. G. Barrell. 2001. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413:848-852.
54. Parkhill, J., B. W. Wren, N. R. Thomson, R. W. Titball, M. T. Holden, M. B. Prentice, M. Sebaihia, K. D. James, C. Churcher, K. L. Mungall, S. Baker, D. Basham, S. D. Bentley, K. Brooks, A. M. Cerdeno-Tarraga, T. Chillingworth, A. Cronin, R. M. Davies, P. Davis, G. Dougan, T. Feltwell, N. Hamlin, S. Holroyd, K. Jagels, A. V. Karlyshev, S. Leather, S. Moule, P. C. Oyston, M. Quail, K. Rutherford, M. Simmonds, J. Skelton, K. Stevens, S. Whitehead, and B. G. Barrell. 2001. Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413:523-527.
55. Phillips, A. P., B. C. Morris, D. Hall, M. Glenister, and J. E. Williams. 1988. Identification of encapsulated and non-encapsulated Yersinia pestis by immunofluorescence tests using polyclonal and monoclonal antibodies. Epidemiol. Infect. 101:59-73.
56. Prentice, M. B., K. D. James, J. Parkhill, S. G. Baker, K. Stevens, M. N. Simmonds, K. L. Mungall, C. Churcher, P. C. Oyston, R. W. Titball, B. W. Wren, J. Wain, D. Pickard, T. T. Hien, J. J. Farrar, and G. Dougan. 2001. Yersinia pestis pFra shows biovar-specific differences and recent common ancestry with a Salmonella enterica serovar Typhi plasmid. J. Bacteriol. 183:2586-2594.
57. Rasko, D. A., G. S. Myers, and J. Ravel. 2005. Visualization of comparative genomic analyses by BLAST score ratio. BMC Bioinformatics 6:2.
58. Sekowska, A., V. Denervaud, H. Ashida, K. Michoud, D. Haas, A. Yokota, and A. Danchin. 2004. Bacterial variations on the methionine salvage pathway. BMC Microbiol. 4:9.
59. Soler Bistué, A. J., D. Birshan, A. P. Tomaras, M. Dandekar, T. Tran, J. Newmark, D. Bui, N. Gupta, K. Hernandez, R. Sarno, A. Zorreguieta, L. A. Actis, and M. E. Tolmasky. 2008. Klebsiella pneumoniae multiresistance plasmid pMET1: similarity with the Yersinia pestis plasmid pCRY and integrative conjugative elements. PLoS One 3:e1800.
60. Song, Y., Z. Tong, J. Wang, L. Wang, Z. Guo, Y. Han, J. Zhang, D. Pei, D. Zhou, H. Qin, X. Pang, Y. Han, J. Zhai, M. Li, B. Cui, Z. Qi, L. Jin, R. Dai, F. Chen, S. Li, C. Ye, Z. Du, W. Lin, J. Wang, J. Yu, H. Yang, J. Wang, P. Huang, and R. Yang. 2004. Complete genome sequence of Yersinia pestis strain 91001, an isolate avirulent to humans. DNA Res. 11:179-197.
61. Summers, D. K., C. W. Beton, and H. L. Withers. 1993. Multicopy plasmid instability: the dimer catastrophe hypothesis. Mol. Microbiol. 8:1031-1038.
62. Thomson, N. R., S. Howard, B. W. Wren, M. T. Holden, L. Crossman, G. L. Challis, C. Churcher, K. Mungall, K. Brooks, T. Chillingworth, T. Feltwell, Z. Abdellah, H. Hauser, K. Jagels, M. Maddison, S. Moule, M. Sanders, S. Whitehead, M. A. Quail, G. Dougan, J. Parkhill, and M. B. Prentice. 2006. The complete genome sequence and comparative genome analysis of the high pathogenicity Yersinia enterocolitica strain 8081. PLoS Genet 2:e206.
63. Torrea, G., V. Chenal-Francisque, A. Leclercq, and E. Carniel. 2006. Efficient tracing of global isolates of Yersinia pestis by restriction fragment length polymorphism analysis using three insertion sequences as probes. J. Clin. Microbiol. 44:2084-2092.
64. Touchman, J. W., D. M. Wagner, J. Hao, S. D. Mastrian, M. K. Shah, A. J. Vogler, C. J. Allender, E. A. Clark, D. S. Benitez, D. J. Youngkin, J. M. Girard, R. K. Auerbach, S. M. Beckstrom-Sternberg, and P. Keim. 2007. A North American Yersinia pestis draft genome sequence: SNPs and phylogenetic analysis. PLoS One 2:e220.
65. Touchon, M., C. Hoede, O. Tenaillon, V. Barbe, S. Baeriswyl, P. Bidet, E. Bingen, S. Bonacorsi, C. Bouchier, O. Bouvet, A. Calteau, H. Chiapello, O. Clermont, S. Cruveiller, A. Danchin, M. Diard, C. Dossat, M. E. Karoui, E. Frapy, L. Garry, J. M. Ghigo, A. M. Gilles, J. Johnson, C. Le Bouguenec, M. Lescat, S. Mangenot, V. Martinez-Jehanne, I. Matic, X. Nassif, S. Oztas, M. A. Petit, C. Pichon, Z. Rouy, C. S. Ruf, D. Schneider, J. Tourret, B. Vacherie, D. Vallenet, C. Medigue, E. P. Rocha, and E. Denamur. 2009. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet. 5:e1000344.
66. Welch, T. J., W. F. Fricke, P. F. McDermott, D. G. White, M. L. Rosso, D. A. Rasko, M. K. Mammel, M. Eppinger, M. J. Rosovitz, D. Wagner, L. Rahalison, J. E. Leclerc, J. M. Hinshaw, L. E. Lindler, T. A. Cebula, E. Carniel, and J. Ravel. 2007. Multiple antimicrobial resistance in plague: an emerging public health risk. PLoS One 2:e309.
67. Welkos, S. L., K. M. Davis, L. M. Pitt, P. L. Worsham, and A. M. Freidlander. 1995. Studies on the contribution of the F1 capsule-associated plasmid pFra to the virulence of Yersinia pestis. Contrib. Microbiol. Immunol. 13:299-305.
68. Wickstrum, J. R., J. M. Skredenske, A. Kolin, D. J. Jin, J. Fang, and S. M. Egan. 2007. Transcription activation by the DNA-binding domain of the AraC family protein RhaS in the absence of its effector-binding domain. J. Bacteriol. 189:4984-4993.
69. Williams, J. E., D. N. Harrison, T. J. Quan, J. L. Mullins, A. M. Barnes, and D. C. Cavanaugh. 1978. Atypical plague bacilli isolated from rodents, fleas, and man. Am. J. Public Health 68:262-264.
70. Winter, C. C., W. B. Cherry, and M. D. Moody. 1960. An unusual strain of Pasteurella pestis isolated from a fatal human case of plague. Bull. W.H.O. 23:408-409.
71. Worsham, P. L., and C. Roy. 2003. Pestoides F, a Yersinia pestis strain lacking plasminogen activator, is virulent by the aerosol route. Adv. Exp. Med. Biol. 529:129-131.
72. Wren, B. W. 2003. The yersiniae-a model genus to study the rapid evolution of bacterial pathogens. Nat. Rev. Microbiol. 1:55-64.
73. Zhou, D., Z. Tong, Y. Song, Y. Han, D. Pei, X. Pang, J. Zhai, M. Li, B. Cui, Z. Qi, L. Jin, R. Dai, Z. Du, J. Wang, Z. Guo, J. Wang, P. Huang, and R. Yang. 2004. Genetics of metabolic variations between Yersinia pestis biovars and the proposal of a new biovar, microtus. J. Bacteriol. 186:5147-5152.
74. Zhou, D., and R. Yang. 2009. Molecular Darwinian evolution of virulence in Yersinia pestis. Infect. Immun. 77:2242-2250.