Transfer of a Traditional Serotyping System (Kauffmann-White) onto a MALDI-TOF-MS Platform for the Rapid Typing of Salmonella Isolates

Mass Spectrometry for Microbial Proteomics

Volumn , Issue , 2010, Pages 463-496

  Bishop, Chloe ^a   Arnold, Catherine ^a   Gharbia, Saheer E ^a  

^a PUBLIC HEALTH ENGLAND   (United Kingdom)

Author keywords

Antigenic analysis Traditional Kauffmann White scheme and its future; DNA sequence based approaches giving flexibility to target selective gene marking for organisms; DNA sequencing using MALDI TOF MS instruments a different approach; O groups identification gene sequences of rfb cluster, for sero specific motifs; Salmonella strain pathogenicity depending on virulence factor combination; Salmonella, a food and water borne pathogen easily disseminated in populations; Salmonellosis, and syndromes gastroenteritis, enteric fevers, septicaemia, focal infections and asymptomatic carrier state; Sequence based methods in determining serotypes; Somatic antigens and Structural Variation of the O Antigen; Traditional serotyping system transfer (Kauffmann White) onto MALDI TOF MS platform for rapid typing of Salmonella isolates

Indexed keywords

EID: 84886549925     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470665497.ch20     Document Type: Chapter

References (137)

1. Agah A , Aghajan M , Mashayekhi F , Amini S , Davis RW , Plummer JD , Ronaghi M , and Griffi n PB: A multi - enzyme model for Pyrosequencing . Nucleic Acids Res 32: e166 , 2004 .
2. Aizawa SI: Flagellar assembly in Salmonella typhimurium . Mol Microbiol 19: 1 - 5, 1996 .
3. Aizawa SI: Bacterial flagella and type III secretion systems . FEMS Microbiol Lett 202: 157 - 164, 2001 .
4. Alcaine SD, Soyer Y, Warnick LD, Su WL, Sukhnanand S, Richards J, Fortes ED, McDonough P, Root TP, Dumas NB, Grohn Y, and Wiedmann M: Multilocus sequence typing supports the hypothesis that cow - and human - associated Salmonella isolates represent distinct and overlapping populations . Appl Environ Microbiol 72: 7575 - 7585, 2006 .
5. Alvarez J, Sota M, Vvanco A, Perales I, Cisterna R, Rementeria R, and Garaizar J: Development of a multiplex PCR technique for detection and epidemiological typing of Salmonella in human clinical samples . J Clin Microbiol 42: 1734 - 1738, 2004 .
6. Baumler AJ: The record of horizontal gene transfer in Salmonella . Trends Microbiol 5: 318 - 322, 1997 .
7. Beltran P, Musser JM, Helmuth R, Farmer JJ, III, Frerichs WM, Wachsmuth IK, Ferris K, McWhorter AC, Wells JG, and Cravioto A: Toward a population genetic analysis of Salmonella: genetic diversity and relationships among strains of serotypes S. choleraesuis, S . derby, S . dublin, S . enteritidis, S . heidelberg, S . infantis, S . newport, and S . typhimurium . Proc Natl Acad Sci USA 85: 7753 - 7757, 1988 .
8. Beltran P, Plock SA, Smith NH, Whittam TS, Old DC, and Selander RK: Reference collection of strains of the Salmonella typhimurium complex from natural populations . J Gen Microbiol 137 ( Pt 3 ): 601 - 606, 1990 .
9. Blake DP, Hillman K, Fenlon DR, and Low JC: Transfer of antibiotic resistance between commensal and pathogenic members of the Enterobacteriaceae under ileal conditions . J Appl Microbiol 95: 428 - 436, 2003 .
10. Blanc - Potard AB and Lafay B: MgtC as a horizontally - acquired virulence factor of intracellular bacterial pathogens: evidence from molecular phylogeny and comparative genomics . J Mol Evol 57: 479 - 486, 2003 .
11. Boyd EF and Brussow H: Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved . Trends Microbiol 10: 521-529, 2002 .
12. Boyd EF and Hartl DL: Analysis of the type 1 pilin gene cluster fi m in Salmonella: its distinct evolutionary histories in the 5 ' and 3 ' regions . J Bacteriol 181: 1301-1308, 1999 .
13. Boyd EF, Wang FS, Whittam TS, and Selander RK: Molecular genetic relationships of the salmonellae . Appl Environ Microbiol 62: 804-808, 1996 .
14. Brenner DJ, Fanning GR, Johnson KE, Citarella RV, and Falkow S: Polynucleotide sequence relationships among members of Enterobacteriaceae . J Bacteriol 98: 637-650, 1969 .
15. Brown PK, Romana LK, and Reeves PR: Molecular analysis of the rfb gene cluster of Salmonella serovar muenchen (strain M67): the genetic basis of the polymorphism between groups C2 and B . Mol Microbiol 6: 1385-1394, 1992 .
16. Chang HR, Loo LH, Jeyaseelan K, Earnest L, and Stackebrandt E: Phylogenetic relationships of Salmonella typhi and Salmonella typhimurium based on 16S rRNA sequence analysis . Int J Syst Bacteriol 47: 1253-1254, 1997 .
17. Choi IG and Kim SH: Global extent of horizontal gene transfer . Proc Natl Acad Sci USA 104: 4489-4494, 2007 .
18. Conner CP, Heithoff DM, Julio SM, Sinsheimer RL, and Mahan MJ: Differential patterns of acquired virulence genes distinguish Salmonella strains . Proc Natl Acad Sci USA 95: 4641-4645, 1998 .
19. Crosa JH, Brenner DJ, Ewing WH, and Falkow S: Molecular relationships among the Salmonelleae . J Bacteriol 115: 307-315, 1973 .
20. Curd H, Liu D, and Reeves PR: Relationships among the O-antigen gene clusters of Salmonella enterica groups B, D1, D2, and D3 . J Bacteriol 180: 1002-1007, 1998 .
21. Dauga C, Zabrovskaia A, and Grimont PA: Restriction fragment length polymorphism analysis of some flagellin genes of Salmonella enterica . J Clin Microbiol 36: 2835-2843, 1998 .
22. de Vries N, Zwaagstra KA, Huis, V, van Knapen F, van Zijderveld FG, and Kusters JG: Production of monoclonal antibodies specifi c for the i and 1,2 flagellar antigens of Salmonella typhimurium and characterization of their respective epitopes . Appl Environ Microbiol 64: 5033-5038, 1998 .
23. Desai M, Threlfall EJ, and Stanley J: Fluorescent amplifi ed-fragment length polymorphism subtyping of the Salmonella enterica serovar enteritidis phage type 4 clone complex . J Clin Microbiol 39: 201-206, 2001 .
24. Ehrich M, Bocker S, and van den BD: Multiplexed discovery of sequence polymorphisms using base-specifi c cleavage and MALDI-TOF MS . Nucleic Acids Res 33: e38, 2005 .
25. Erridge C, Bennett-Guerrero E, and Poxton IR: Structure and function of lipopolysaccharides . Microbes Infect 4: 837-851, 2002 .
26. Fakhr MK, Nolan LK, and Logue CM: Multilocus sequence typing lacks the discriminatory ability of pulsed-fi eld gel electrophoresis for typing Salmonella enterica serovar Typhimurium. J Clin Microbiol 43: 2215-2219, 2005 .
27. Fitzgerald C, Collins M, van Duyne S, Mikoleit M, Brown T, and Fields P: Multiplex, bead-based suspension array for the molecular determination of common Salmonella serogroups . J Clin Microbiol E.pub ahead of print, 2007 .
28. Fitzgerald C, Gheesling L, Collins M, and Fields PI: Sequence analysis of the rfb loci encoding biosynthesis of the S. enterica O17 and O18 antigens: serogroup-specifi c identifi cation by PCR . Appl Environ Microbiol 72: 7949-7953, 2006 .
29. Fitzgerald C, Sherwood R, Gheesling LL, Brenner FW, and Fields PI: Molecular analysis of the rfb O antigen gene cluster of Salmonella enterica serogroup O:6,14 and development of a serogroup-specifi c PCR assay . Appl Environ Microbiol 69: 6099-6105, 2003 .
30. Frankel G, Newton SM, Schoolnik GK, and Stocker BA: Unique sequences in region VI of the flagellin gene of Salmonella typhi . Mol Microbiol 3: 1379-1383, 1989 .
31. Fraser GM and Hughes C: Swarming motility . Curr Opin Microbiol 2: 630-635, 1999 .
32. Gophna U, Ron EZ, and Graur D: Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events . Gene 312: 151-163, 2003 .
33. Groisman EA and Ochman H: How Salmonella became a pathogen . Trends Microbiol 5: 343-349, 1997 .
34. Guard-Petter J, Keller LH, Rahman MM, Carlson RW, and Silvers S: A novel relationship between O-antigen variation, matrix formation, and invasiveness of Salmonella enteritidis . Epidemiol Infect 117: 219-231, 1996 .
35. Guerra B, Landeras E, Gonzalez-Hevia MA, and Mendoza MC: A three-way ribotyping scheme for Salmonella serotype Typhimurium and its usefulness for phylogenetic and epidemiological purposes . J Med Microbiol 46: 307-313, 1997 .
36. Guiney DG, Fang FC, Krause M, Libby S, Buchmeier NA, and Fierer J: Biology and clinical signifi-cance of virulence plasmids in Salmonella serovars . Clin Infect Dis 21 ( Suppl. 2): S146-S151, 1995.
37. Gupta S and Maiden MC: Exploring the evolution of diversity in pathogen populations . Trends Microbiol 9: 181-185, 2001 .
38. Hacker J and Kaper JB: Pathogenicity islands and the evolution of microbes . Annu Rev Microbiol 54: 641-679, 2000 .
39. Hanafusa T, Saito K, Tominaga A, and Enomoto M: Nucleotide sequence and regulated expression of the Salmonella fljA gene encoding a repressor of the phase 1 flagellin gene . Mol Gen Genet 236: 260-266, 1993 .
40. Hanage WP, Fraser C, and Spratt BG: Sequences, sequence clusters and bacterial species . Philos Trans R Soc Lond, Ser B 361: 1917-1927, 2006 .
41. Hansen-Wester I and Hensel M: Salmonella pathogenicity islands encoding type III secretion systems . Microbes Infect 3: 549-559, 2001 .
42. Hansen-Wester I and Hensel M: Genome-based identifi cation of chromosomal regions specifi c for Salmonella spp . Infect Immun 70: 2351-2360, 2002 .
43. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, Eng JK, Akira S, Underhill DM, and Aderem A: The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5 . Nature 410: 1099-1103, 2001 .
44. He XS, Rivkina M, Stocker BA, and Robinson WS: Hypervariable region IV of Salmonella gene fliCd encodes a dominant surface epitope and a stabilizing factor for functional flagella . J Bacteriol 176: 2406-2414, 1994 .
45. Health Protection Agency . Salmonella in humans (excluding S. Typhi & S. Paratyphi) reported to the Health Protection Agency Centre for Infections, England and Wales, 1981-2006. http:// www.hpa.org.uk/infections/topics_az/salmonella/data_human.htm . 2007 .
46. Health Protection Agency . Salmonella in humans (excluding S. typhi; S. Paratyphi). Faecal and lower gastrointestinal tract isolates reported to the Health Protection Agency Centre for Infections. England and Wales, 1990-2008. http://www.hpa.org.uk/infections/topics_az/salmonella/ data_human.htm . 2009 .
47. Helander IM, Moran AP, and Makela PH: Separation of two lipopolysaccharide populations with different contents of O-antigen factor 122 in Salmonella enterica serovar typhimurium . Mol Microbiol 6: 2857-2862, 1992 .
48. Hensel M, Shea JE, Baumler AJ, Gleeson C, Blattner F, and Holden DW: Analysis of the boundaries of Salmonella pathogenicity island 2 and the corresponding chromosomal region of Escherichia coli K-12 . J Bacteriol 179: 1105-1111, 1997 .
49. Homma M, Fujita H, Yamaguchi S, and Iino T: Regions of Salmonella typhimurium flagellin essential for its polymerization and excretion . J Bacteriol 169: 291-296, 1987 .
50. Hong Y, Liu T, Hofacre C, Maier M, White DG, Ayers S, Wang L, and Maurer JJ: A restriction fragment length polymorphism-based polymerase chain reaction as an alternative to serotyping for identifying Salmonella serotypes . Avian Dis 47: 387-395, 2003 .
51. Honisch C, Chen Y, Mortimer C, Arnold C, Schmidt O, van den BD, Cantor CR, Shah HN, and Gharbia SE: Automated comparative sequence analysis by base-specifi c cleavage and mass spectrometry for nucleic acid-based microbial typing . Proc Natl Acad Sci USA 104: 10649-10654, 2007 .
52. House D, Bishop A, Parry C, Dougan G, and Wain J: Typhoid fever: pathogenesis and disease . Curr Opin Infect Dis 14: 573-578, 2001 .
53. Ibrahim GF, Fleet GH, Lyons MJ, and Walker RA: Production of potent Salmonella H antisera by immunization with polymeric flagellins . J Clin Microbiol 22: 347-351, 1985 .
54. Jensen SO and Reeves PR: Molecular evolution of the GDP-mannose pathway genes ( manB and manC ) in Salmonella enterica . Microbiology 147: 599-610, 2001 .
55. Ji WS, Hu JL, Qiu JW, Pan BR, Peng DR, Shi BL, Zhou SJ, Wu KC, and Fan DM: Relationship between genotype and phenotype of flagellin C in Salmonella . World J Gastroenterol 7: 864-867, 2001 .
56. Jiang XM, Neal B, Santiago F, Lee SJ, Romana LK, and Reeves PR: Structure and sequence of the rfb (O antigen) gene cluster of Salmonella serovar typhimurium (strain LT2) . Mol Microbiol 5: 695-713, 1991 .
57. Joys TM: The covalent structure of the phase-1 flagellar fi lament protein of Salmonella typhimurium and its comparison with other flagellins . J Biol Chem 260: 15 758-15 761, 1985 .
58. Joys TM and Schodel F: Epitope mapping of the d flagellar antigen of Salmonella muenchen . Infect Immun 59: 3330-3332, 1991 .
59. Jurinke C, van den BD, Cantor CR, and Koster H: The use of MassARRAY technology for high throughput genotyping . Adv Biochem Eng Biotechnol 77: 57-74, 2002 .
60. Kanto S, Okino H, Aizawa S, and Yamaguchi S: Amino acids responsible for flagellar shape are distributed in terminal regions of flagellin . J Mol Biol 219: 471-480, 1991 .
61. Keenleyside WJ, Perry M, Maclean L, Poppe C, and Whitfi eld C: A plasmid-encoded rfbO:54 gene cluster is required for biosynthesis of the O:54 antigen in Salmonella enterica serovar Borreze . Mol Microbiol 11: 437-448, 1994 .
62. Kidgell C, Reichard U, Wain J, Linz B, Torpdahl M, Dougan G, and Achtman M: Salmonella typhi, the causative agent of typhoid fever, is approximately 50,000 years old . Infect Genet Evol 2: 39-45, 2002 .
63. Kilger G and Grimont PA: Differentiation of Salmonella phase 1 flagellar antigen types by restriction of the amplifi ed fliC gene . J Clin Microbiol 31: 1108-1110, 1993 .
64. Kingsley RA and Baumler AJ: Host adaptation and the emergence of infectious disease: the Salmonella paradigm . Mol Microbiol 36: 1006-1014, 2000 .
65. Kingsley RA and Baumler AJ: Pathogenicity islands and host adaptation of Salmonella serovars . Curr Top Microbiol Immunol 264: 67-87, 2002 .
66. Konstantinidis KT, Ramette A, and Tiedje JM: Towards a more robust assessment of intra-species diversity using fewer genetic markers . Appl Environ Microbiol 2006 .
67. Kotetishvili M, Stine OC, Kreger A, Morris JG, Jr, and Sulakvelidze A: Multilocus sequence typing for characterization of clinical and environmental Salmonella strains . J Clin Microbiol 40: 1626-1635, 2002 .
68. Lan R and Reeves PR: Gene transfer is a major factor in bacterial evolution . Mol Biol Evol 13: 47-55, 1996 .
69. Lawson AJ, Stanley J, Threlfall EJ, and Desai M: Fluorescent amplifi ed fragment length polymorphism subtyping of multiresistant Salmonella enterica serovar Typhimurium DT104 . J Clin Microbiol 42: 4843-4845, 2004 .
70. Lee CA: Pathogenicity islands and the evolution of bacterial pathogens . Infect Agents Dis 5: 1-7, 1996 .
71. Lee SJ, Romana LK, and Reeves PR: Sequence and structural analysis of the rfb (O antigen) gene cluster from a group C1 Salmonella enterica strain . J Gen Microbiol 138 ( Pt 9 ): 1843-1855, 1992 .
72. Lerouge I and Vanderleyden J: O-antigen structural variation: mechanisms and possible roles in animal/plant-microbe interactions . FEMS Microbiol Rev 26: 17-47, 2002 .
73. Li J, Nelson K, McWhorter AC, Whittam TS, and Selander RK: Recombinational basis of serovar diversity in Salmonella enterica . Proc Natl Acad Sci USA 91: 2552-2556, 1994 .
74. Li J, Smith NH, Nelson K, Crichton PB, Old DC, Whittam TS, and Selander RK: Evolutionary origin and radiation of the avian-adapted non-motile salmonellae . J Med Microbiol 38: 129-139, 1993 .
75. Liu D, Verma NK, Romana LK, and Reeves PR: Relationships among the rfb regions of Salmonella serovars A, B, and D . J Bacteriol 173: 4814-4819, 1991 .
76. Liu SL, Hessel A, and Sanderson KE: Genomic mapping with I-Ceu I, an intron-encoded endonuclease specifi c for genes for ribosomal RNA, in Salmonella spp., Escherichia coli, and other bacteria . Proc Natl Acad Sci USA 90: 6874-6878, 1993 .
77. Looney RJ and Steigbigel RT: Role of the Vi antigen of Salmonella typhi in resistance to host defense in vitro . J Lab Clin Med 108: 506-516, 1986 .
78. Ludwig W and Schleifer KH: Bacterial phylogeny based on 16S and 23S rRNA sequence analysis . FEMS Microbiol Rev 15: 155-173, 1994 .
79. Luk JM, Kongmuang U, Reeves PR, and Lindberg AA: Selective amplifi cation of abequose and paratose synthase genes ( rfb ) by polymerase chain reaction for identifi cation of Salmonella major serogroups (A, B, C2, and D) . J Clin Microbiol 31: 2118-2123, 1993 .
80. Macnab RM: Genetics and biogenesis of bacterial flagella . Annu Rev Genet 26: 131-158, 1992 .
81. Macnab RM: Flagella and motility . In: E schericia coli and S almonella: Cellular and Molecular Biology ( Neidhardt FC, Curtiss R, Ingraham JL, and Low KB eds). Washington DC, ASM Press, 1996, pp 123-145 .
82. Marcus SL, Brumell JH, Pfeifer CG, and Finlay BB: Salmonella pathogenicity islands: big virulence in small packages . Microbes Infect 2: 145-156, 2000 .
83. Mashayekhi F and Ronaghi M: Analysis of read length limiting factors in Pyrosequencing chemistry . Anal Biochem 363: 275-287, 2007 .
84. Masten BJ and Joys TM: Molecular analyses of the S almonella g flagellar antigen complex. J Bacteriol 176: 2771, 1994 .
85. Matic I, Taddei F, and Radman M: Genetic barriers among bacteria . Trends Microbiol 4: 69-72, 1996 .
86. Mayeux PR: Pathobiology of lipopolysaccharide . J Toxicol Environ Health 51: 415-435, 1997 .
87. McConnell MR, Oakes KR, Patrick AN, Mills DM: Two functional O-polysaccharide polymerase wzy ( rfc ) genes are present in the rfb gene cluster of Group E1 Salmonella enterica serovar Anatum . FEMS Microbiol Lett 199: 235-240, 2001 .
88. McQuiston JR, Parrenas R, Ortiz-Rivera M, Gheesling L, Brenner F, and Fields PI: Sequencing and comparative analysis of flagellin genes fliC, fljB, and flpA from Salmonella . J Clin Microbiol 42: 1923-1932, 2004 .
89. Mortimer CK, Peters TM, Gharbia SE, Logan JM, and Arnold C: Towards the development of a DNA-sequence based approach to serotyping of Salmonella enterica . BMC Microbiol 4: 31, 2004 .
90. Murase T, Okitsu T, Suzuki R, Morozumi H, Matsushima A, Nakamura A, and Yamai S: Evaluation of DNA fi ngerprinting by PFGE as an epidemiologic tool for Salmonella infections . Microbiol Immunol 39: 673-676, 1995 .
91. Newton SM, Wasley RD, Wilson A, Rosenberg LT, Miller JF, and Stocker BA: Segment IV of a Salmonella flagellin gene specifi es flagellar antigen epitopes . Mol Microbiol 5: 419-425, 1991.
92. Nghiem HO, Himmelspach K, and Mayer H: Immunochemical and structural analysis of the O polysaccharides of Salmonella zuerich [1,9,27,(46)] . J Bacteriol 174: 1904-1910, 1992 .
93. Nnalue NA and Lindberg AA: O-antigenic determinants in Salmonella species of serogroup C1 are expressed in distinct immunochemical populations of chains . Microbiology 143 ( Pt 2 ): 653-662, 1997 .
94. Ochman H and Wilson AC: Evolution in bacteria: evidence for a universal substitution rate in cellular genomes . J Mol Evol 26: 74-86, 1987 .
95. Ohl ME and Miller SI: Salmonella: a model for bacterial pathogenesis . Annu Rev Med 52: 259-274, 2001 .
96. Parish CR, Wistar R, and Ada G: Cleavage of bacterial flagellin with cyanogen bromide: antigenic properties of the protein fragments . Biochem J 113: 501-506, 1969 .
97. Parker CT and Guard-Petter J: Contribution of flagella and invasion proteins to pathogenesis of Salmonella enterica serovar enteritidis in chicks . FEMS Microbiol Lett 204: 287-291, 2001 .
98. Peters TM and Threlfall EJ: Single-enzyme amplifi ed fragment length polymorphism and its applicability for Salmonella epidemiology . Syst Appl Microbiol 24: 400-404, 2001 .
99. Popoff MY: Antigenic Formulas of Salmonella serovars . Paris, Institute Pasteur, 2001 .
100. Porwollik S McClelland M: Lateral gene transfer in Salmonella . Microbes Infect 5: 977-989, 2003 .
101. Porwollik S, Wong RM, and McClelland M: Evolutionary genomics of Salmonella: gene acquisitions revealed by microarray analysis . Proc Natl Acad Sci USA 99: 8956-8961, 2002 .
102. Reeves P: Evolution of S almonella O antigen variation by interspecifi c gene transfer on a large scale . Trends Genet 9: 17-22, 1993 .
103. Reeves PR: Variation in O-antigens, niche-specifi c selection bacterial populations . FEMS Microbiol Lett 79: 509-516, 1992 .
104. Reeves PR, Hobbs M, Valvano MA, Skurnik M, Whitfi eld C, Coplin D, Kido N, Klena J, Maskell D, Raetz CR, and Rick PD: Bacterial polysaccharide synthesis and gene nomenclature . Trends Microbiol 4: 495-503, 1996 .
105. Ridley AM, Threlfall EJ, and Rowe B: Genotypic characterization of Salmonella enteritidis phage types by plasmid analysis, ribotyping, and pulsed-fi eld gel electrophoresis . J Clin Microbiol 36: 2314-2321, 1998 .
106. Ronaghi M, Karamohamed S, Pettersson B, Uhlen M, and Nyren P: Real-time DNA sequencing using detection of pyrophosphate release . Anal Biochem 242: 84-89, 1996 .
107. Rychlik I, Gregorova D, and Hradecka H: Distribution and function of plasmids in Salmonella enterica . Vet Microbiol 112: 1-10, 2006 .
108. Salmon D and Smith T: The bacterium of swine-plague . Am Microscop J 7: 204-205, 1886 .
109. Samatey FA, Imada K, Nagashima S, Vonderviszt F, Kumasaka T, Yamamoto M, and Namba K: Structure of the bacterial flagellar protofi lament and implications for a switch for supercoiling . Nature 410: 331-337, 2001 .
110. Samuel G and Reeves P: Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly . Carbohydr Res 338: 2503-2519, 2003 .
111. Sanger F, Nicklen S, and Coulson AR: DNA sequencing with chain-terminating inhibitors . Proc Natl Acad Sci USA 74: 5463-5467, 1977 .
112. Schmidt H and Hensel M: Pathogenicity islands in bacterial pathogenesis . Clin Microbiol Rev 17: 14-56, 2004 .
113. Scott F, Threlfall J, and Arnold C: Genetic structure of S almonella revealed by fragment analysis . Int J Syst Evol Microbiol 52: 1701-1713, 2002 .
114. Selander RK, Smith NH, Li J, Beltran P, Ferris KE, Kopecko DJ, and Rubin FA: Molecular evolutionary genetics of the cattle-adapted serovar Salmonella dublin . J Bacteriol 174: 3587-3592, 1992 .
115. Silverman M, Zieg J, Hilmen M, and Simon M: Phase variation in Salmonella: genetic analysis of a recombinational switch . Proc Natl Acad Sci USA 76: 391-395, 1979 .
116. Smith NH and Selander RK: Molecular genetic basis for complex flagellar antigen expression in a triphasic serovar of Salmonella . Proc Natl Acad Sci USA 88: 956-960, 1991 .
117. Sonne-Hansen J and Jenabian SM: Molecular serotyping of Salmonella: identifi cation of the phase 1 H antigen based on partial sequencing of the fliC gene . APMIS 113: 340-348, 2005 .
118. Stock JB, Surette MG, McCleary WR, and Stock AM: Signal transduction in bacterial chemotaxis . J Biol Chem 267: 19753-19756, 1992 .
119. Sukhnanand S, Alcaine S, Warnick LD, Su WL, Hof J, Craver MP, McDonough P, Boor KJ, and Wiedmann M: DNA sequence-based subtyping and evolutionary analysis of selected Salmonella enterica serotypes . J Clin Microbiol 43: 3688-3698, 2005 .
120. Szekely E and Simon M: Homology between the invertible deoxyribonucleic acid sequence that controls flagellar-phase variation in Salmonella sp. and deoxyribonucleic acid sequences in other organisms . J Bacteriol 148: 829-836, 1981 .
121. Szekely E and Simon M: DNA sequence adjacent to flagellar genes and evolution of flagellar-phase variation . J Bacteriol 155: 74-81, 1983 .
122. Tasteyre A, Karjalainen T, Avesani V, Delmee M, Collignon A, Bourlioux P, and Barc MC: Phenotypic and genotypic diversity of the flagellin gene ( fliC ) among Clostridium diffi cile isolates from different serogroups . J Clin Microbiol 38: 3179-3186, 2000 .
123. Threlfall EJ, Hampton MD, Chart H, and Rowe B: Use of plasmid profi le typing for surveillance of Salmonella enteritidis phage type 4 from humans, poultry and eggs . Epidemiol Infect 112: 25-31, 1994 .
124. Vazquez-Torres A, Jones-Carson J, Baumler AJ, Falkow S, Valdivia R, Brown W, Le M, Berggren R, Parks WT, and Fang FC: Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes . Nature 401: 804-808, 1999 .
125. Vernikos GS, Thomson NR, and Parkhill J: Genetic flux over time in the Salmonella lineage . Genome Biol 8: R100, 2007 .
126. Wain J, House D, Pickard D, Dougan G, and Frankel G: Acquisition of virulence-associated factors by the enteric pathogens Escherichia coli and Salmonella enterica . Philos Trans R Soc Lond, Ser B 356: 1027-1034, 2001 .
127. Wang L, Andrianopoulos K, Liu D, Popoff MY, and Reeves PR: Extensive variation in the O-antigen gene cluster within one Salmonella enterica serogroup reveals an unexpected complex history . J Bacteriol 184: 1669-1677, 2002 .
128. Wang L, Romana LK, and Reeves PR: Molecular analysis of a Salmonella enterica group E1 rfb gene cluster: O antigen and the genetic basis of the major polymorphism . Genetics 130: 429-443, 1992 .
129. Wang L, Rothemund D, Curd H, and Reeves PR: Species-wide variation in the Escherichia coli flagellin (H-antigen) gene . J Bacteriol 185: 2936-2943, 2003 .
130. Wang Q, Suzuki A, Mariconda S, Porwollik S, and Harshey RM: Sensing wetness: a new role for the bacterial flagellum . EMBO J 24: 2034-2042, 2005 .
131. Weisburg WG, Barns SM, Pelletier DA, and Lane DJ: 16S ribosomal DNA amplifi cation for phylogenetic study . J Bacteriol 173: 697-703, 1991 .
132. Whittam TS and Bumbaugh AC: Inferences from whole-genome sequences of bacterial pathogens . Curr Opin Genet Dev 12: 719-725, 2002 .
133. Winokur PL: Molecular epidemiological techniques for Salmonella strain discrimination . Front Biosci 8: c14-c24, 2003 .
134. World Health Organisation . Salmonella . http://www.who.int/topics/salmonella/en/ . 2007 .
135. Xiang SH, Haase AM, Reeves Variation of the rfb gene clusters in Salmonella enterica . J Bacteriol 175: 4877
136. Yu LSL and Fung DYC: Use if selective motility enrichment to isolate foodborne pathogens: A review . J Rapid Methods Automat Microbiol 2: 167, 1993 .
137. Zeng H, Carlson AQ, Guo Y, Yu Y, Collier-Hyams LS, Madara JL, Gewirtz AT, and Neish AS: Flagellin is the major proinflammatory determinant of enteropathogenic Salmonella . J Immunol 171: 3668-3674, 2003 .