A population genetics-based and phylogenetic approach to understanding the evolution of virulence in the genus Listeria

Applied and Environmental Microbiology

Volumn 76, Issue 18, 2010, Pages 6085-6100

  Den Bakker, Henk C ^a   Bundrant, Brittany N ^a   Fortes, Esther D ^a   Orsi, Renato H ^a   Wiedmann, Martin ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ECOLOGICAL NICHE; LISTERIA SPECIES; LISTERIA SPP; LOWER AVERAGE; MONOCYTOGENES; MULTILOCUS SEQUENCE TYPING; PHYLOGENETIC ANALYSIS; PHYLOGENETIC APPROACH; POPULATION BOTTLENECKS; POPULATION GENETICS; VIRULENCE GENE;

BIOLOGY; DISEASES; ECOLOGY;

LISTERIA;

BACTERIAL PROTEIN; BACTERIAL TOXIN; HEAT SHOCK PROTEIN; HEMOLYSIN; HLYA PROTEIN, LISTERIA MONOCYTOGENES; PRFA PROTEIN, LISTERIA MONOCYTOGENES; PRIMER DNA; TRANSLATION TERMINATION FACTOR;

ANCESTRY; BACTERIUM; CLADISTICS; DIVERGENCE; EVOLUTIONARY BIOLOGY; GENETIC ANALYSIS; NICHE; PATHOGENICITY; PHYLOGENY; POPULATION GENETICS; SAPROTROPHY; SELECTION; STOCHASTICITY; TAXONOMY; VIRULENCE;

ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; CLASSIFICATION; DNA SEQUENCE; EVOLUTION; GENETICS; LISTERIA; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYLOGENY; POPULATION GENETICS; SEQUENCE ALIGNMENT; SPECIES DIFFERENCE; STATISTICAL MODEL; VIRULENCE;

BACTERIAL PROTEINS; BACTERIAL TOXINS; BASE SEQUENCE; BAYES THEOREM; BIOLOGICAL EVOLUTION; DNA PRIMERS; GENETICS, POPULATION; HEAT-SHOCK PROTEINS; HEMOLYSIN PROTEINS; LIKELIHOOD FUNCTIONS; LISTERIA; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PEPTIDE TERMINATION FACTORS; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; VIRULENCE;

LISTERIA; LISTERIA GRAYI; LISTERIA INNOCUA; LISTERIA IVANOVII; LISTERIA MONOCYTOGENES; LISTERIA SEELIGERI; LISTERIA WELSHIMERI;

EID: 77956803817     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00447-10     Document Type: Article

References (77)

1. Achtman, M. 2008. Evolution, population structure, and phylogeography of genetically monomorphc bacterial pathogens. Annu. Rev. Microbiol. 62: 53-70.
2. Achtman, M., G. Morelli, P. Zhu, T. Wirth, I. Diehl, B. Kusecek, A. J. Vogler, D. 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. U. S. A. 101: 17837-17842.
3. Bierne, H., C. Sabet, N. Personnic, and P. Cossart. 2007. Internalins: a complex family of leucine-rich repeat-containing proteins in Listeria monocytogenes. Microbes Infect. 9: 1156-1166.
4. Boerlin, P., J. Rocourt, F. Grimont, P. Grimont, C. Jacquet, and J. C. Piflaretti. 1992. Listeria Ivanova subsp. londoniensis subsp. nov. Int. J. Syst. Bacteriol. 42: 69-73.
5. Boerlin, P., J. Rocourt, and J. C. Piffaretti. 1991. Taxonomy of the genus Listeria by using multilocus enzyme electrophoresis. Int. J. Syst. Bacteriol. 41: 59-64.
6. Brown, E. W., M. K. Mammel, J. E. LeClerc, and T. A. Cebula. 2003. Limited boundaries for extensive horizontal gene transfer among Salmonella pathogens. Proc. Natl. Acad. Sci. U. S. A. 100: 15676-15681.
7. Bruen, T. C., H. Philippe, and D. Bryant. 2006. A simple and robust statistical test for detecting the presence of recombination. Genetics 172: 2665-2681.
8. Bubert, A., S. Köhler, and W. Goebel. 1992. The homologous and heterologous regions within the lap gene allow genus- and species-specific identification of Listeria spp. by polymerase chain reaction. Appl. Environ. Microbiol. 58: 2625-2632.
9. Cal, S., and M. Wiedmann. 2001. Characterization of the prfA virulence gene cluster insertion site in non-hemolytic Listeria spp.: probing the evolution of the Listeria virulence gene island. Curr. Microbiol. 43: 271-277.
10. Curiale, M., and C. Lewus. 1994. Detection of Listeria monocytogenes in samples containing Listeria innocua. J. Food Prot. 57: 1048-1051.
11. den Bakker, H. C., X. Didelot, E. Fortes, K. K. Nightingale, and M. Wiedmann. 2008. Lineage specific recombination rates and microevolution in Listeria monocytogenes. BMC Evol. Biol. 8: 277.
12. Didelot, X., M. Barker, D. Falush, and F. G. Priest. 2009. Evolution of pathogenicity in the Bacillus cereus group. Syst. Appl. Microbiol. 32: 81-90.
13. Domínguez-Bernal, G., S. Müller-Altrock, B. Gonzdlez-Zorn, M. Scortti, P. Herrmann, H. J. Monzó, L. Lacharme, J. Kreft, and J. A. Vázquez-Boland. 2006. A spontaneous genomic deletion in Listeria ivanovii identifies LIPI-2. a species-specific pathogenicity island encoding sphingomyelinase and numerous internalins. Mol. Microbiol. 59: 415-432.
14. Drummond, A. J., S. Y. M. Ho, M. J. Phillips, and A. Rambaut. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4: e88.
15. Drummond, A. J., and A. Rambaut. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7: 214.
16. Falush, D., M. Stephens, and J. Pritchard. 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567-1587.
17. Felsenstein, J. 1985. Confidence-limits on phytogenies: an approach using the bootstrap. Evolution 39: 783-791.
18. Filliol, I., A. S. Motiwala, M. Cavatore, W. Qi, M. H. Hazbón, M. Bobadilla del Valle, J. Fyfe, L. García-García, N. Rastogi, C. Sola, T. Zozio, M. I. Guerrero, C. I. León, J. Crabtree, S. Angiuoli, K. D. Eisenach, R. Durmaz, M. L. Joloba, A. Rendón, J. Sifuentes-Osornio, A. Ponce de León, M. D. Cave, R. Fleischmann, T. S. Whittam, and D. Alland. 2006. Global phytogeny of Mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J. Bacteriol. 188: 759-772.
19. Fredslund, J., L. Schauser, L. H. Madsen, N. Sandal, and J. Stougaard. 2005. PriFi: using a multiple alignment of related sequences to find primers for amplification of homologs. Nucleic Acids Res. 33: W516-W520.
20. Furrer, B., U. Candrian, C. Hoefelein, and J. Luethy. 1991. Detection and identification of Listeria monocytogenes in cooked sausage products and in milk by in vitro amplification of haemolysin gene fragments. J. Appl. Bacteriol. 70: 372-379.
21. Glaser, P., L. Frangeul, C. Buchrieser, C. Rusniok, A Amend, F. Baquero, P. Berche, H. Bloecker, P. Brandt, T. Chakraborty, A. Charbit, F. Chetouani, E. Couve, A. de Daruvar, P. Dehoux, E. Domann, G. Dominguez-Bernal, E. Duchaud, L. Durant, O. Dussurget, K. D. Entian, H. Fsihi, F. Garcia-del Portillo, P. Garrido, L. Gautier, W. Goebel, N. Gomez-Lopez, T. Hain, J. Haut, D. Jackson, L. M. Jones, U. Kaerst, J. Kreft, M. Kuhn, F. Kunst, G. Kurapkat, E. Madueno, A. Maitournam, J. M. Vicente, E. Ng, H. Nedjari, G. Nordsiek, S. Novella, B. de Pablos, J. C. Perez-Diaz, R. Purcell, B. Remmel, M. Rose, T. Schlueter, N. Simoes, A. Tierrez, J. A. Vazquez-Boland, H. Voss, J. Wehland, and P. Cossart. 2001. Comparative genomics of Listeria species. Science 294: 849-852.
22. Graves, L. M., L. O. Helsel, A. G. Steigerwalt, R. E. Morey, M. I. Daneshvar, S. E. Roof, R. H. Orsi, E. D. Fortes, S. R. Millilo, H. C. den Bakker, M. Wiedmann, B. Swaminathan, and B. D. Sauders. 10 August 2009, posting date. Listeria marthii sp. nov., isolated from the natural environment, Finger Lakes National Forest. Int. J. Syst. Evol. Microbiol. 60: 1280-1288.
23. Gray, M., R. Zadoks, E. Fortes, B. Dogan, S. Cai, Y. Chen, V. Scott, D. Gombas, K. Boor, and M. Wiedmann. 2004. Listeria monocytogenes isolates from foods and humans form distinct but overlapping populations. Appl. Environ. Microbiol. 70: 5833-5841.
24. Groves, R. D., and H. J. Welshimer. 1977. Separation of pathogenic from apathogenic Listeria monocytogenes by three in vitro reactions. J. Clin. Microbiol. 5: 559-563.
25. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phytogenies by maximum likelihood. Syst. Biol. 52: 696-704.
26. Hacker, J., G. Blum-Oehler, I. Mühldorfer, and H. Tschäpe. 1997. Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol. Microbiol. 23: 1089-1097.
27. Hain, T., C. Steinweg, and T. Chakraborty. 2006. Comparative and functional genomics of Listeria spp. J. Biotechnol. 126: 37-51.
28. Hain, T., C. Steinweg, C. T. Kuenne, A. Billion, R. Ghai, S. S. Chatterjee, E. Domann, U. Karst, A. Goesmann, T. Bekel, D. Bartels, O. Kaiser, F. Meyer, A. Puhler, B. Weisshaar, J. Wehland, C. Liang, T. Dandekar, R. Lampidis, J. Kreft, W. Goebel, and T. Chakraborty. 2006. Whole-genome sequence of Listeria welshimeri reveals common steps in genome reduction with Listeria innocua as compared to Listeria monocytogenes. J. Bacteriol. 188: 7405-7415.
29. Jakobsen, I. B., and S. Easteal. 1996. A program for calculating and displaying compatibility matrices as an aid in determining reticulate evolution in molecular sequences. Comput. Appl. Biosci. 12: 291-295.
30. Jeffers, G., J. Bruce, P. McDonough, J. Scarlett, K. Boor, and M. Wiedmann. 2001. Comparative genetic characterization of Listeria monocytogenes isolates from human and animal listeriosis cases. Microbiology 147: 1095-1104.
31. Johnson, J., K. Jinneman, G. Stelma, B. G. Smith, D. Lye, J. Messer, J. Ulaszek, L. Evsen, S. Gendel, R. W. Bennett, B. Swaminathan, J. Pruckler, A. Steigerwalt, S. Kathariou, S. Yildirim, D. Volokhov, A. Rasooly, V. Chizhikov, M. Wiedmann, E. Fortes, R. E. Duvall, and A. D. Hitchins. 2004. Natural atypical Listeria innocua strains with Listeria monocytogenes pathogenicity island 1. genes. Appl. Environ. Microbiol. 70: 4256-4266.
32. Lan, R., and P. R. Reeves. 2001. When does a clone deserve a name? A perspective on bacterial species based on population genetics. Trends Microbiol. 9: 419-424.
33. Leclercq, A., D. Clermont, C. Bizet, P. Grimont, A. Le Flèche-Mntéos, S. Roche, C. Buchrieser, V. Cadet-Daniel, A. Le Monnier, M. Lecuit, and F. Allerberger. 13 November 2009, posting date. Listeria rocourtiae sp. nov. Int. J. Syst. Evol. Microbiol. [Epub ahead of print.]
34. Lessing, M. P., G. D. Curtis, and I. C. Bowler. 1994. Listeria ivanovii infection. J. Infect. 29: 230-231.
35. Maddison, D. R., and W. P. Maddison. 2005. MACCLADE version 4.08. Sinauer Associates Inc., Sunderland, MA.
36. Maddison, W. P., and D. R. Maddison. 2009. Mesquite: a modular system for evolutionary analysis, 2.72 ed.
37. Maynard Smith, J. 1992. Analyzing the mosaic structure of genes. J. Mol. Evol. 34: 126-129.
38. Maynard Smith, J., N. H. Smith, M. O'Rourke, and B. G. Spratt. 1993. How clonal are bacteria? Proc. Natl. Acad. Sci. U. S. A. 90: 4384-4388.
39. McLauchlin, J. 1997. The identification of Listeria species. Int. J. Food Microbiol. 38: 77-81.
40. Milillo, S. R., and M. Wiedmann. 2009. Contributions of six lineage-specific internalin-like genes to invasion efficiency of Listeria monocytogenes. Foodborne Pathog. Dis. 6: 57-70.
41. Müller, A. A., M. W. Schmid, O. Meyer, and F. G. Meussdoerffer. 2010. Listeria seeligeri isolates from food processing environments form two phylogenetic lineages. Appl. Environ. Microbiol. 76: 3044-3047.
42. Nelson, K. E., D. E. Fouts, E. F. Mongodin, J. Ravel, R. T. DeBoy, J. F. Kolonay, D. A. Rasko, S. V. Angiuoli, S. R. Gill, I. T. Paulsen, J. Peterson, O. White, W. C. Nelson, W. Merman, M. J. Beanan, L. M. Brinkac, S. C. Daugherty, R. J. Dodson, A. S. Durkin, R. Madupu, D. H. Haft, J. Selengut, S. Van Aken, H. Khouri, N. Fedorova, H. Forberger, B. Tran, S. Kathariou, L. D. Wonderling, G. A. Uhlich, D. O. Bayles, J. B. Luchansky, and C. M. Fraser. 2004. Whole genome comparisons of serotype 4b and l/2a strains of the food-borne pathogen Listeria monocytogenes reveal new insights into the core genome components of this species. Nucleic Acids Res. 32: 2386-2395.
43. Nielsen, R. 2001. Statistical tests of selective neutrality in the age of genomics. Heredity 86: 641-647. (Pubitemid 32930824)
44. Nightingale, K., L. Bovell, A. Grajczyk, and M. Wiedmann. 2007. Combined sigB allelic typing and multiplex PCR provide improved discriminatory power and reliability for Listeria monocytogenes molecular serotyping. J. Microbiol. Methods 68: 52-59.
45. Nightingale, K., K. Windham, and M. Wiedmann. 2005. Evolution and molecular phytogeny of Listeria monocytogenes isolated from human and animal listeriosis cases and foods. J. Bacteriol. 187: 5537-5551.
46. Orsi, R. H., Q. Sun, and M. Wiedmann. 2008. Genome-wide analyses reveal lineage specific contributions of positive selection and recombination to the evolution of Listeria monocytogenes. BMC Evol. Biol. 8: 233.
47. Petran, R., and K. Swanson. 1993. Simultaneous growth of Listeria monocytogenes and Listeria innocua. J. Food Prot. 56: 616-618.
48. Piffaretti, J. C., H. Kressebuch, M. Aeschbacher, J. Bille, E. Bannerman, J. M. Musser, R. K. Selander, and J. Rocourt. 1989. Genetic characterization of clones of the bacterium. Listeria monocytogenes causing epidemic disease. Proc. Natl. Acad. Sci. U. S. A. 86: 3818-3822.
49. Posada, D., and K. A. Crandall. 2001. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc. Natl. Acad. Sci. U. S. A. 98: 13757-13762.
50. Posada, D., and K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818.
51. Ragon, M., T. Wirth, F. Hollandt, R. Lavenir, M. Lecuit, A. L. Monnier, and S. Brisse. 2008. A new perspective on Listeria monocytogenes evolution. PLoS Pathog. 4: el000146.
52. Rajabian, T., B. Gavicherla, M. Heisig, S. Müller-Altrock, W. Goebel, S. Gray-Owen, and K. Ireton. 2009. The bacterial virulence factor InlC perturbs apical cell junctions and promotes cell-to-cell spread of Listeria. Nat. Cell Biol. 11: 1212-1218.
53. Ramage, C. P., J. C. Low, J. McLauchlin, and W. Donachie. 1999. Characterisation of Listeria ivanovii isolates from the UK using pulsed-field gel electrophoresis. FEMS Microbiol. Lett. 170: 349-353.
54. Rasmussen, O. F., P. Skouboe, L. Dons, L. Rossen, and J. E. Olsen. 1995. Listeria monocytogenes exists in at least three evolutionary lines: evidence from flagellin, invasive associated protein and listeriolysin O genes. Microbiology 141: 2053-2061.
55. Roberts, A., K. Nightingale, G. Jeff'ers, E. Fortes, J. M. Kongo, and M. Wiedmann. 2006. Genetic and phenotypic characterization of Listeria monocytogenes lineage III. Microbiology 152: 685-693.
56. Rocourt, J., F. Grimont, P. Grimont, and H. Seeliger. 1982. DNA relatedness among serovars af Listeria monocytogenes sensu lato. Curr. Microbiol. 7: 383-388.
57. Roumagnac, P., F. X. Weill, C. Dolecek, S. Baker, S. Brisse, N. T. Chinh, T. A. Le, C. J. Acosta, J. Farrar, G. Dougan, and M. Achtman. 2006. Evolutionary history of Salmonella typhi. Science 314: 1301-1304.
58. Rozas, J., J. Sánchez-DelBarrio, X. Messeguer, and R. Rozas. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497. (Pubitemid 38016658)
59. Sauders, B. D., M. Z. Durak, E. Fortes, K. Windham, Y. Schukken, A. J. Lembo, Jr., B. Akey, K. K. Nightingale, and M. Wiedmann. 2006. Molecular characterization of Listeria monocytogenes from natural and urban environments. J. Food Prot. 69: 93-105.
60. Sawyer, S. A. 1999. GENECONV: a computer package for the statistical detection of gene conversion. Department of Mathematics, Washington University in St. Louis, St. Louis, MO. http://www.math.wustl.edu/~sawyer/geneconv/.
61. Schmid, M., E. Ng, R. Lampidis, M. Emmerth, M. Walcher, J. Kreft, W. Goebel, M. Wagner, and K. Schleifer. 2005. Evolutionary history of the genus Listeria and its virulence genes. Syst. Appl. Microbiol. 28: 1-18.
62. Simonsen, K., G. Churchill, and C. Aquadro. 1995. Properties of statistical tests of neutrality for DNA polymorphism data. Genetics 141: 413-429.
63. Stuart, S., and H. Welshimer. 1974. Taxonomie reexamination of Listeria Pirie and transfer of Listeria grayi and Listeria murrayi to a new genus, Murraya. Int. J. Syst. Evol. Microbiol. 24: 177-185.
64. Swofford, D. L. 2002. PAUP: Phylogenetic Analysis Using Parsimony ( and other methods), version. 4.0. Sinauer Associates Inc., Sunderland, MA.
65. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595. (Pubitemid 19274682)
66. Vazquez-Boland, J. A., G. Dominguez-Bernal, B. Gonzalez-Zorn, J. Kreft, and W. Goebel. 2001. Pathogenicity islands and virulence evolution in Listeria. Microbes Infect. 3: 571-584.
67. Vazquez-Boland, J. A., M. Kuhn, P. Berche, T. Chakraborty, G. DominguezBernal, W. Goebel, B. Gonzalez-Zorn, J. Wehland, and J. Kreft. 2001. Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 14: 584-640.
68. Volokhov, D., S. Duperrier, A. Neverov, J. George, C. Buchrieser, and A. Hitchins. 2007. The presence of the internal in gene in natural atypically hemolytic Listeria innocua strains suggests descent from L. monocytogenes. Appl. Environ. Microbiol. 73: 1928-1939.
69. Volokhov, D., J. George, C. Anderson, R. Duvall, and A. Hitchins. 2006. Discovery of natural atypical nonhemolytic Listeria seeligeri isolates. Appl. Environ. Microbiol. 72: 2439-2448.
70. Walk, S. T., E. W. Alm, L. M. Calhoun, J. M. Mladonicky, and T. S. Whittam. 2007. Genetic diversity and population structure of Escherichia coli isolated from freshwater beaches. Environ. Microbiol. 9: 2274-2288.
71. Ward, T., L. Gorski, M. Borucki, R. Mandrell, J. Hutchins, and K. Pupedis. 2004. Intraspecific phytogeny and lineage group identification based on the prfA virulence gene cluster of Listeria monocytogenes. J. Bacteriol. 186: 4994-5002.
72. Ward, T. J., T. F. Ducey, T. Usgaard, K. A. Dunn, and J. P. Bielawski. 2008. Multilocus genotyping assays for single nucleotide polymorphism-based subtyping af Listeria monocytogenes isolates. Appl. Environ. Microbiol. 74: 7629-7642.
73. Whelan, S. 2008. Spatial and temporal heterogeneity in nucleotide sequence evolution. Mol. Biol. Evol. 25: 1683-1694.
74. Wong, W. S., Z. Yang, N. Goldman, and R. Nielsen. 2004. Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. Genetics 168: 1041-1051.
75. Yang, Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24: 1586-1591.
76. Yule, G. U. 1925. A mathematical theory of evolution, based on the conclusions of Dr. JC Willis, FRS. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1925: 21-87.
77. Zhang, J., R. Nielsen, and Z. Yang. 2005. Evaluation of an improved branchsite likelihood method for detecting positive selection at the molecular level. Mol. Biol. Evol. 22: 2472-2479.