Genome wide evolutionary analyses reveal serotype specific patterns of positive selection in selected Salmonella serotypes

BMC Evolutionary Biology

Volumn 9, Issue 1, 2009, Pages

  Soyer, Yeim ^a   Orsi, Renato H ^a   Rodriguez Rivera, Lorraine D ^a   Sun, Qi ^a   Wiedmann, Martin ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OUTER MEMBRANE PROTEIN; BACTERIAL DNA;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CONTROLLED STUDY; GENE; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC ANALYSIS; HOMOLOGOUS RECOMBINATION; HOST; MODEL; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OMPC GENE; SALMONELLA; SEROTYPE; CLASSIFICATION; COMPARATIVE GENOMIC HYBRIDIZATION; DNA SEQUENCE; GENETIC RECOMBINATION; GENETIC SELECTION; GENETICS; SEROTYPING;

ANIMALIA; BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA ENTERICA;

COMPARATIVE GENOMIC HYBRIDIZATION; DNA, BACTERIAL; EVOLUTION, MOLECULAR; GENES, BACTERIAL; GENOME, BACTERIAL; RECOMBINATION, GENETIC; SALMONELLA; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA; SEROTYPING;

EID: 72049088798     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-9-264     Document Type: Article

References (76)

1. Salmonella nomenclature-Guest commentary. FW Brenner RG Villar FJ Angulo R Tauxe B Swaminathan, J Clin Microbiol 2000 38 7 2465 2467 10878026
2. Host adapted serotypes of Salmonella enterica. S Uzzau DJ Brown T Wallis S Rubino G Leori S Bernard J Casadesus DJ Platt JE Olsen, Epidemiol Infect 2000 125 2 229 255 10.1017/S0950268899004379 11117946
3. Salmonella typhi, the causative agent of typhoid fever, is approximately 50,000 years old. C Kidgell U Reichard J Wain B Linz M Torpdahl G Dougan M Achtman, Infect Genet Evol 2002 2 1 39 45 10.1016/S1567-1348(02)00089-8 12797999
4. The Genome of Salmonella enterica Serovar Typhi. S Baker G Dougan, Clin Infect Dis 2007 45 Suppl 1 29 S33 10.1086/518143 17582565
5. Comparison of genome degradation in Paratyphi A and Typhi, human-restricted serovars of Salmonella enterica that cause typhoid. M McClelland KE Sanderson SW Clifton P Latreille S Porwollik A Sabo R Meyer T Bieri P Ozersky M McLellan CR Harkins CY Wang C Nguyen A Berghoff G Elliott S Kohlberg C Strong FY Du J Carter C Kremizki D Layman S Leonard H Sun L Fulton W Nash T Miner P Minx K Delehaunty C Fronick V Magrini M Nhan W Warren L Florea J Spieth RK Wilson, Nat Gen 2004 36 12 1268 1274 10.1038/ng1470 (Pubitemid 39577934)
6. Discrimination within phenotypically closely related definitive types of Salmonella enterica serovar typhimurium by the multiple amplification of phage locus typing technique. IL Ross MW Heuzenroeder, J Clin Microbiol 2005 43 4 1604 1611 10.1128/JCM.43.4.1604-1611.2005 15814973
7. Transmission routes of Salmonella Typhimurium DT 104 between 14 cattle and pig herds in Denmark demonstrated by molecular fingerprinting. B Langvad MN Skov E Rattenborg JE Olsen DL Baggesen, J Appl Microbiol 2006 101 4 883 890 10.1111/j.1365-2672.2006.02992.x 16968300
8. A severe Salmonella enterica serotype Paratyphi B infection in a child related to a pet turtle, Trachemys scripta elegans. N Nagano S Oana Y Nagano Y Arakawa, Jpn J Infect Dis 2006 59 2 132 134 16632917
9. Foodborne disease trends and reports. B Swaminathan P Gerner-Smidt, Foodborne Pathog Dis 2006 3 3 220 221 10.1089/fpd.2006.3.220 16972769 (Pubitemid 44519320)
10. The genome sequence of Salmonella enterica serovar Choleraesuis, a highly invasive and resistant zoonotic pathogen. CH Chiu P Tang CS Chu SN Hu QY Bao J Yu YY Chou HS Wang YS Lee, Nucleic Acids Res 2005 33 5 1690 1698 10.1093/nar/gki297 15781495
11. The temperature-sensing protein TlpA is repressed by PhoP and dispensable for virulence of Salmonella enterica serovar Typhimurium in mice. O Gal-Mor Y Valdez BB Finlay, Microb Infect 2006 8 8 2154 2162 10.1016/j.micinf.2006.04.015 (Pubitemid 44311592)
12. Adaptive evolution of bacterial metabolic networks by horizontal gene transfer. C Pal B Papp MJ Lercher, Nat Genet 2005 37 12 1372 1375 10.1038/ng1686 16311593
13. Lateral gene transfer in Salmonella. S Porwollik M McClelland, Microbes Infect 2003 5 11 977 989 10.1016/S1286-4579(03)00186-2 12941390
14. Integration of horizontally transferred genes into regulatory interaction networks takes many million years. MJ Lercher C Pal, Mol Biol Evol 2008 25 3 559 567 10.1093/molbev/msm283 18158322
15. Pathogenicity islands in bacterial pathogenesis. H Schmidt M Hensel, Clin Microbiol Rev 2004 17 1 14 56 10.1128/CMR.17.1.14-56.2004 14726454
16. Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. NR Thomson DJ Clayton D Windhorst G Vernikos S Davidson C Churcher MA Quail M Stevens MA Jones M Watson A Barron A Layton D Pickard RA Kingsley A Bignell L Clark B Harris D Ormond Z Abdellah K Brooks I Cherevach T Chillingworth J Woodward H Norberczak A Lord C Arrowsmith K Jagels S Moule K Mungall M Sanders S Whitehead JA Chabalgoity D Maskell T Humphrey M Roberts PA Barrow G Dougan J Parkhill, Genome Res 2008 18 10 1624 1637 10.1101/gr.077404. 108 18583645
17. Characterization of Salmonella enterica subspecies I genovars by use of microarrays. S Porwollik EF Boyd C Choy P Cheng L Florea E Proctor M McClelland, J Bacteriol 2004 186 17 5883 5898 10.1128/JB.186.17.5883-5898.2004 15317794
18. Genome-wide analyses reveal lineage specific contributions of positive selection and recombination to the evolution of Listeria monocytogenes. RH Orsi Q Sun M Wiedmann, BMC Evol Biol 2008 8 233 254 10.1186/1471-2148-8-233 18700032
19. Comparative analysis of tandem T7-like promoter containing regions in enterobacterial genomes reveals a novel group of genetic islands. ZH Chen TD Schneider, Nucleic Acids Res 2006 34 4 1133 1147 10.1093/nar/gkj511 16493139
20. Evolution of the core and pan-genome of Streptococcus: positive selection, recombination, and genome composition. T Lefebure MJ Stanhope, Genome Biol 2007 8 5 71 10.1186/gb-2007-8-5-r71 17475002
21. Comparative genomics of Salmonella enterica serovar typhi strains Ty2 and CT18. W Deng SR Liou G Plunkett GF Mayhew DJ Rose V Burland V Kodoyianni DC Schwartz FR Blattner, J Bacteriol 2003 185 7 2330 2337 10.1128/JB.185.7.2330- 2337.2003 12644504
22. Pervasive, genome-wide positive selection leading to functional divergence in the bacterial genus Campylobacter. T Lefebure MJ Stanhope, Genome Res 2009 19 7 1224 1232 10.1101/gr.089250.108 19304960
23. Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach. SL Chen CS Hung J Xu CS Reigstad V Magrini A Sabo D Blasiar T Bieri RR Meyer P Ozersky JR Armstrong RS Fulton JP Latreille J Spieth TM Hooton ER Mardis SJ Hultgren JI Gordon, Proc Natl Acad Sci USA 2006 103 15 5977 5982 10.1073/pnas.0600938103 16585510
24. Genes under positive selection in Escherichia coli. L Petersen JP Bollback M Dimmic M Hubisz R Nielsen, Genome Res 2007 17 9 1336 1343 10.1101/gr.6254707 17675366
25. The rate of adaptive evolution in enteric bacteria. J Charlesworth A Eyre-Walker, Mol Biol Evol 2006 23 7 1348 1356 10.1093/molbev/msk025 16621913 (Pubitemid 43992336)
26. Salmonella pathogenicity islands: big virulence in small packages. SL Marcus JH Brumell CG Pfeifer BB Finlay, Microb Infect 2000 2 2 145 156 10.1016/S1286-4579(00)00273-2 (Pubitemid 30154704)
27. The role of horizontal gene transfer in the evolution of selected foodborne bacterial pathogens. BG Kelly A Vespermann DJ Bolton, Food Chem Toxicol 2009 47 5 951 968 10.1016/j.fct.2008.02.006 18420329
28. OrthoMCL: identification of ortholog groups for eukaryotic genomes. L Li CJ Stoeckert Jr DS Roos, Genome Res 2003 13 9 2178 2189 10.1101/gr.1224503 12952885
29. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. JD Thompson DG Higgins TJ Gibson, Nucleic Acids Res 1994 22 22 4673 4680 10.1093/nar/22.22.4673 7984417
30. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. M Suyama D Torrents P Bork, Nucleic Acids Res 2006 34 Web Server 609 612 10.1093/nar/gkl315 16845082
31. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. TA Hall, Nucl Acids Symp Ser 1999 41 95 98
32. Phylogenetic evidence for frequent positive selection and recombination in the meningococcal surface antigen PorB. R Urwin EC Holmes AJ Fox JP Derrick MC Maiden, Mol Biol Evol 2002 19 10 1686 1694 12270895
33. Strong positive selection and recombination drive the antigenic variation of the PilE protein of the human pathogen Neisseria meningitidis. TD Andrews T Gojobori, Genetics 2004 166 1 25 32 10.1534/genetics.166.1.25 15020403
34. Phylogenetic evidence for adaptive evolution of dengue viruses in nature. SS Twiddy CH Woelk EC Holmes, J Gen Virol 2002 83 Pt 7 1679 1689 12075087
35. A scan for positively selected genes in the genomes of humans and chimpanzees. R Nielsen C Bustamante AG Clark S Glanowski TB Sackton MJ Hubisz A Fledel-Alon DM Tanenbaum D Civello TJ White J Sninsky MD Adams M Cargill, PLoS Biol 2005 3 6 170 10.1371/journal.pbio.0030170 15869325
36. Positive selection and expression divergence following gene duplication in the sunflower CYCLOIDEA gene family. MA Chapman JH Leebens-Mack JM Burke, Mol Biol Evol 2008 25 7 1260 1273 10.1093/molbev/msn001 18390478
37. Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. WS Wong Z Yang N Goldman R Nielsen, Genetics 2004 168 2 1041 1051 10.1534/genetics.104.031153 15514074
38. PAML: a program package for phylogenetic analysis by maximum likelihood. Z Yang, Comput Appl Biosci 1997 13 5 555 556 9367129
39. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. JZ Zhang R Nielsen ZH Yang, Mol Biol Evol 2005 22 12 2472 2479 10.1093/molbev/msi237 16107592
40. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Z Yang R Nielsen N Goldman AM Pedersen, Genetics 2000 155 1 431 449 10790415
41. Statistical tests for detecting gene conversion. S Sawyer, Mol Biol Evol 1989 6 5 526 538 2677599
42. Analyzing the Mosaic Structure of Genes. JM Smith, J Mol Evol 1992 34 2 126 129 1556748
43. A simple and robust statistical test for detecting the presence of recombination. TC Bruen H Philippe D Bryant, Genetics 2006 172 4 2665 2681 10.1534/genetics.105.048975 16489234
44. A program for calculating and displaying compatibility matrices as an aid in determining reticulate evolution in molecular sequences. IB Jakobsen S Easteal, Comput Appl Biosci 1996 12 4 291 295 8902355
45. Recombination in evolutionary genomics. D Posada KA Crandall EC Holmes, Annu Rev Genet 2002 36 75 97 10.1146/annurev.genet.36.040202.111115 12429687
46. Evaluation of methods for detecting recombination from DNA sequences: empirical data. D Posada, Mol Biol Evol 2002 19 5 708 717 11961104
47. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. D Posada KA Crandall, Proc Natl Acad Sci USA 2001 98 24 13757 13762 10.1073/pnas.241370698 11717435
48. EMBOSS: the European Molecular Biology Open Software Suite. P Rice I Longden A Bleasby, Trends Genet 2000 16 6 276 277 10.1016/S0168-9525(00)02024-2 10827456
49. Controlling the False Discovery Rate: a Practical and Powerful Approach to Multiple Testing. Y Benjamini Y Hochberg, J Royal Statis Soc B 1995 57 1 289 300
50. Statistical significance for genomewide studies. JD Storey R Tibshirani, Proc Natl Acad Sci USA 2003 100 16 9440 9445 10.1073/pnas.1530509100 12883005
51. Salmonella surveillance: Annual Summary, 2004. Center for Disease Control and Prevention (CDC), Atlanta, Georgia: US Department of Health and Human Services, CDC http://www.cdc.gov/ncidod/dbmd/phlisdata/salmonella.htm
52. Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. M Anisimova R Nielsen Z Yang, Genetics 2003 164 3 1229 1236 12871927
53. Complete genome sequence of Salmonella enterica serovar typhimurium LT2. M McClelland KE Sanderson J Spieth SW Clifton P Latreille L Courtney S Porwollik J Ali M Dante FY Du SF Hou D Layman S Leonard C Nguyen K Scott A Holmes N Grewal E Mulvaney E Ryan H Sun L Florea W Miller T Stoneking M Nhan R Waterston RK Wilson, Nature 2001 413 6858 852 856 10.1038/35101614 11677609
54. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. J Parkhill G Dougan KD James NR Thomson D Pickard J Wain C Churcher KL Mungall SD Bentley MTG Holden M Sebaihia S Baker D Basham K Brooks T Chillingworth P Connerton A Cronin P Davis RM Davies L Dowd N White J Farrar T Feltwell N Hamlin A Haque TT Hien S Holroyd K Jagels A Krogh TS Larsen S Leather S Moule P O'Gaora C Parry M Quail K Rutherford M Simmonds J Skelton K Stevens S Whitehead BG Barrell, Nature 2001 413 6858 848 852 10.1038/35101607 11677608
55. Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. EV Koonin YI Wolf, Nucleic Acids Res 2008 36 6688 6719 10.1093/nar/gkn668 18948295
56. Codon bias and base composition are poor indicators of horizontally transferred genes. LB Koski RA Morton GB Golding, Mol Biol Evol 2001 18 3 404 412 11230541
57. A bimodal pattern of relatedness between the Salmonella Paratyphi A and Typhi genomes: convergence or divergence by homologous recombination? X Didelot M Achtman J Parkhill NR Thomson D Falush, Genome Res 2007 17 1 61 68 10.1101/gr.5512906 17090663
58. Pathogenicity islands and the evolution of microbes. J Hacker JB Kaper, Annual Rev Microbiol 2000 54 641 679 10.1146/annurev.micro.54.1.641 (Pubitemid 30835922)
59. Distribution of "classic" virulence factors among Salmonella spp. AJ van Asten JE van Dijk, FEMS Immunol Med Microbiol 2005 44 3 251 259 10.1016/j.femsim.2005.02.002 15907446
60. Identification of host-specific colonization factors of Salmonella enterica serovar Typhimurium. E Morgan JD Campbell SC Rowe J Bispham MP Stevens AJ Bowen PA Barrow DJ Maskell TS Wallis, Mol Microbiol 2004 54 4 994 1010 10.1111/j.1365-2958.2004.04323.x 15522082
61. Contribution of SPI-4 genes to the virulence of Salmonella enterica. T Kiss E Morgan G Nagy, FEMS Microbiol Lett 2007 275 1 153 159 10.1111/j.1574-6968.2007.00871.x 17711458
62. Identification of a pathogenicity island required for Salmonella enteropathogenicity. MW Wood MA Jones PR Watson S Hedges TS Wallis EE Galyov, Mol Microbiol 1998 29 3 883 891 10.1046/j.1365-2958.1998.00984.x 9723926
63. Salmonella effectors within a single pathogenicity island are differentially expressed and translocated by separate type III secretion systems. LA Knodler J Celli WD Hardt BA Vallance C Yip BB Finlay, Mol Microbiol 2002 43 5 1089 1103 10.1046/j.1365-2958.2002.02820.x 11918798
64. Salmonella Pathogenicity Islands. E Morgan, Salmonella: Molecular Biology and Pathogenesis Norfolk: Horizon Bioscience, Rhen M, Maskell D, Mastroeni P, Threlfall J, 2007 67 88
65. The Salmonella enterica subspecies I specific centisome 7 genomic island encodes novel protein families present in bacteria living in close contact with eukaryotic cells. A Folkesson S Lofdahl S Normark, Res Microbiol 2002 153 8 537 545 10.1016/S0923-2508(02)01348-7 12437215
66. Differentially evolved genes of Salmonella pathogenicity islands: insights into the mechanism of host specificity in Salmonella. SM Eswarappa J Janice AG Nagarajan SV Balasundaram G Karnam NM Dixit D Chakravortty, PLoS ONE 2008 3 12 3829 10.1371/journal.pone.0003829 19050757
67. Genetic determinants and polymorphisms specific for human-adapted serovars of Salmonella enterica that cause enteric fever. DM Tracz H Tabor M Jerome LK Ng MW Gilmour, J Clin Microbiol 2006 44 6 2007 2018 10.1128/JCM.02630-05 16757591
68. NrdI essentiality for class Ib ribonucleotide reduction in Streptococcus pyogenes. I Roca E Torrents M Sahlin I Gibert BM Sjoberg, J Bacteriol 2008 190 14 4849 4858 10.1128/JB.00185-08 18502861
69. Nucleotide biosynthesis is critical for growth of bacteria in human blood. S Samant H Lee M Ghassemi J Chen JL Cook AS Mankin AA Neyfakh, PLoS Pathog 2008 4 2 37 10.1371/journal.ppat.0040037 18282099
70. DNA repair is more important than catalase for Salmonella virulence in mice. NA Buchmeier SJ Libby Y Xu PC Loewen J Switala DG Guiney FC Fang, J Clin Invest 1995 95 3 1047 1053 10.1172/JCI117750 7883952
71. The porin OmpC of Salmonella typhimurium mediates adherence to macrophages. RS Negm TG Pistole, Can J Microbiol 1999 45 8 658 669 10.1139/cjm-45-8-658 10528398
72. OmpC is the receptor for Gifsy-1 and Gifsy-2 bacteriophages of Salmonella. TD Ho JM Slauch, J Bacteriol 2001 183 4 1495 1498 10.1128/JB.183.4.1495-1498.2001 11157969
73. Adaptive evolution and recombination of Rickettsia antigens. FM Jiggins, J Mol Evol 2006 62 1 99 110 10.1007/s00239-005-0080-9 16408241
74. The porin and the permeating antibiotic: a selective diffusion barrier in Gram-negative bacteria. JM Pages CE James M Winterhalter, Nat Rev Microbiol 2008 6 12 893 903 10.1038/nrmicro1994 18997824
75. Antimicrobial resistance in nontyphoidal Salmonella. SD Alcaine LD Warnick M Wiedmann, J Food Protect 2007 70 3 780 790 17388077
76. Loss of OmpC porin in a strain of Salmonella typhimurium causes increased resistance to cephalosporins during therapy. AA Medeiros TF O'Brien EY Rosenberg H Nikaido, J Infect Dis 1987 156 5 751 757 2821125