Hierarchical clustering of genetic diversity associated to different levels of mutation and recombination in Escherichia coli: A study based on Mexican isolates

Infection, Genetics and Evolution

Volumn 13, Issue 1, 2013, Pages 187-197

  González González, Andrea ^a   Sánchez Reyes, Luna L ^a,c   Delgado Sapien, Gabriela ^b   Eguiarte, Luis E ^a   Souza, Valeria ^a  

^a INSTITUTO DE ECOLOGÍA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Clonal complex; Epidemiological surveillance; Escherichia coli; Homologous recombination; Point mutation; Population structure

Indexed keywords

ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATION; CLONAL VARIATION; CONTROLLED STUDY; ESCHERICHIA COLI; GENE CLUSTER; GENEALOGY; GENETIC VARIABILITY; HOMOLOGOUS RECOMBINATION; MEXICO; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POINT MUTATION; POPULATION GENETICS; POPULATION STRUCTURE; PRIORITY JOURNAL; SPECIES DIFFERENTIATION; UNINDEXED SEQUENCE;

ANIMALS; CLUSTER ANALYSIS; ESCHERICHIA COLI; GENES, BACTERIAL; GENETIC VARIATION; HOMOLOGOUS RECOMBINATION; HUMANS; MEXICO; MOLECULAR SEQUENCE DATA; MULTILOCUS SEQUENCE TYPING; MUTATION; PHYLOGENY;

AVES; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MAMMALIA;

EID: 84870557623     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2012.09.003     Document Type: Article

References (88)

1. Achtman M., Zurth K., Morelli G., Torrea G., Guiyoule A., Carniel E. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. USA 1999, 96:14043-14048.
2. Allen H.K., Donato J., Wang H.H., Cloud-Hansen K.A., Davies J., Handelsman J. Call of the wild: antibiotic resistance genes in natural environments. Nat. Rev. Microbiol. 2010, 8:251-259.
3. Bergholz P.W., Noar J.D., Buckely D.H. Environmental patterns are imposed on the population structure of Escherichia coli after fecal deposition. Appl. Environ. Microbiol. 2011, 77:129-211.
4. Bielaszewska M., Middendorf B., Köck R., Friedrich A.W., Fruth A., Karch H., Schmidt M.A., Mellmann A. Shiga toxin-negative attaching and effacing Escherichia coli: distinct clinical associations with bacterial phylogeny and virulence traits and inferred in-host pathogen evolution. Clin. Infect. Dis. 2008, 47:208-217.
5. Buckee C.O., Jolley K.A., Recker M., Penman B., Kriz P., Gupta S., Maiden M.C.J. Role of selection in the emergence of lineages and the evolution of virulence in Neisseria meningitidis. Proc. Natl. Acad. Sci. USA 2008, 105:15082-15087.
6. Caugant D.A., Levin B.R., Selander R.K. Genetic diversity and temporal variation in the E. coli population of a human host. Genetics 1981, 98:467-490.
7. Clermont O., Bonacorsi S., Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl. Environ. Microbiol. 2000, 66:4555-4558.
8. Clermont O., Olier M., Hoede C., Diancourt L., Brisse S., Keroudean M., Glodt J., et al. Animal and human pathogenic Escherichia coli strains share common genetic backgrounds. Infect. Genet. Evol. 2011, 11:654-662.
9. Cohan F.M., Kopac S.M. Microbial genomics: E. coli relatives out of doors and out of body. Curr. Biol. 2011, 21:R587-R589.
10. Cohan F.M., Perry E.B. A systematics for discovering the fundamental units of bacterial diversity. Curr. Biol. 2007, 17:R373-R386.
11. Denamur E., Picard B., Tenaillon O. Population genetics of pathogenic Escherichia coli. Bacterial Population Genetics in Infectious Diseases 2010, 269-286. Wiley-Blackwell, West Sussex, United Kingdom. D.A. Robinson, D. Falush, E.J. Feil (Eds.).
12. Didelot X., Falush D. Inference of bacterial microevolution using multilocus sequence data. Genetics 2007, 175:1251-1266.
13. Didelot X., Meric G., Falush D., Darling A.E. Impact of homologous and non-homologous recombination in the genomic evolution of Escherichia coli. BMC Genomics 2012, 13:256.
14. Duriez P., Clermont O., Bonacorsi S., Bingen E., Chaventré A., Elion J., Picard B., Denamur E. Commensal Escherichia coli isolates are phylogenetically distributed among geographically distinct human populations. Microbiology 2001, 147:1671-1676.
15. Escobar-Páramo P., Clermont O., Blanc-Potard A.B., Bui H., Le Bouguénec C., Denamur E. A specific genetic background is required for acquisition and expression of virulence factors in Escherichia coli. Mol. Biol. Evol. 2004, 21:1085-1094.
16. Estrada-Garcia T., Lopez-Saucedo C., Thompson-Bonilla R., et al. Association of diarrheagenic Escherichia coli pathotypes with infection and diarrhea among Mexican children and association of atypical enteropathogenic E. coli with acute diarrhea. J. Clin. Microbiol. 2009, 47:93-98.
17. Evanno G., Regnaut S., Goudet J. Detecting the number of clusters of individuals using the software structure: a simulation study. Mol. Ecol. 2005, 14:2611-2620.
18. Ewing B., Hillier L., Wendi M.C., Green P. Base-calling of automated sequencer traces using phred I. Accuracy assessment. Genome. Res. 1998, 8:175-185.
19. Excoffier L., Laval G., Schneider S. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol. Bioinform. Online 2005, 1:47-50.
20. Feil E.J. Small change: keeping pace with microevolution. Nat. Rev. Microbiol. 2004, 2:483-495.
21. Feil E.J. Linkage, selection, and the clonal complex. Bacterial Population Genetics in Infectious Diseases 2010, 19-35. Wiley-Blackwell, West Sussex, United Kingdom. D.A. Robinson, D. Falush, E.J. Feil (Eds.).
22. Feil E.J., Holmes E.C., Bessen D.E., Chan M.S., Day N.P., Enright M.C., Goldstein R., Hood D.W., Kalia A., Moore C.E., et al. Recombination within natural populations of pathogenic bacteria: short term empirical estimates and long-term phylogenetic consequences. Proc. Natl. Acad. Sci. USA 2001, 98:182-187.
23. Feil E.J., Li B.C., Aanensen D.M., Hanage W.P., Spratt B.G. EBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J. Bacteriol. 2004, 186:1518-1530.
24. Fraser C., Hanage W.P., Spratt B.G. Recombination and the nature of bacterial speciation. Science 2007, 315:476-480.
25. Gelman A., Rubin D.B. Inference from iterative simulation using multiple sequences. Statist. Sci. 1992, 7:457-472.
26. Gordon D., Abajian C., Green P. Consed: a graphical tool for sequence finishing. Genome Res. 1998, 8:195-202.
27. Gordon D.M., Clermont O., Tolley H., Denamur E. Assigning Escherichia coli strains to phylogenetic groups: multi-locus sequence typing versus the triplex method. Environ. Microbiol. 2008, 10:2484-2496.
28. Gordon D.M., Cowling A. The distribution and genetic structure of Escherichia coli Australian vertebrates: host and geographic effects. Microbiology 2003, 12:3575-3586.
29. Goullet P., Picard B. Comparative electrophoretic polymorphism of esterases and other enzymes in Escherichia coli. J. Gen. Microbiol. 1989, 135:135-143.
30. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 1999, 41:95-98.
31. Haubold B., Hudson R.R. LIAN 3.0: detecting linkage disequilibrium in multilocus data. Bioinformatics 2000, 16:847-849.
32. Herzer P., Inouye S., Inouye M., Whittam T.S. Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J. Bacteriol. 1990, 172:6175-6181.
33. Holmes E.C., Urwin R., Maiden M.C. The influence of recombination on the population structure and evolution of the human pathogen Neisseria meningitidis. Mol. Biol. Evol. 1999, 16:741-749.
34. Jaureguy F., Landraud L., Passet V., Diancourt L., Frapy E., Guigon G., Carbonnelle E., Lortholary O., Clermont O., Denamur E., et al. Phylogenetic and genomic diversity of human bacteremic Escherichia coli strains. BMC Genomics 2008, 9:560-573.
35. Johnson J.R., Menard M.E., Lauderdale T.-L., Kosmidis C.H., Gordon D., Collignon P., Maslow J.N., Tambic-Andrasevic A., Kuskowski M.A. Global distribution and epidemiologic associations of Escherichia coli clonal group A, 1998-2007. Emerg. Infect. Dis. 2011, 17:2001-2009. Trans-Global Initiative for Antimicrobial Resistance Analysis Investigators.
36. Johnson J.R., Owens K.L., Clabots C.R., Weissman S.J., Cannon S.B. Phylogenetic relationships among clonal groups of extraintestinal pathogenic Escherichia coli as assessed by multi-locus sequence analysis. Microbes Infect. 2006, 8:1702-1713.
37. Kaper J.B., Nataro J.P., Mobley H.L. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2004, 2:123-140.
38. Koeppel A., Perry E.B., Sikorski J., Krizanc D., Warner W.A., Ward D.M., Rooney A.P., Brambilla E., Connor N., Ratcliff R.M., et al. Identifying the fundamental units of bacterial diversity: a paradigm shift to incorporate ecology into bacterial systematics. Proc. Natl. Acad. Sci. USA 2008, 105:2504-2509.
39. Lau S.H., Reddy S., Cheesbrough J., Bolton F.J., Willshaw G., Cheasty T., Fox A.J., Upton M. Major uropathogenic Escherichia coli strain isolated in the northwest of England identified by multilocus sequence typing. J. Clin. Microbiol. 2008, 46:1076-1080.
40. Le Gall T., Clermont O., Gouriou S., Picard B., Nassif X., et al. Extraintestinal virulence is a coincidental by-product of commensalism in B2 phylogenetic group Escherichia coli strains. Mol. Biol. Evol. 2007, 24:2373-2384.
41. Leopold S.R., Sawyer S.A., Whittam T.S., Tarr P.I. Obscured phylogeny and possible recombinational dormancy in Escherichia coli. BMC Evol. Biol. 2011, 11:183-191.
42. Levin B.R. Periodic selection, infectious gene exchange and the genetic structure of E. coli populations. Genetics 1981, 99:1-23.
43. López-Saucedo C., Cerna J.F., Villegas-Sepulveda N., Thompson R., Velazquez F.R., Torres J., Tarr P.I., Estrada-García T. Single multiplex polymerase chain reaction to detect diverse loci associated with diarrheagenic Escherichia coli. Emerg. Infect. Dis. 2003, 9:127-131.
44. Luo C., Walk S.T., Gordon D.M., Feldgarden M., Tiedje J.M., Konstantinidis K.T. Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species. Proc. Natl. Acad. Sci. USA 2011, 108:7200-7205.
45. Maiden M.C.J., Bygraves J.A., Feil E., Morelli G., Russell J.E., Urwin R., Zhang Q., Zhou J., Zurth K., Caugant D.A., Feavers I.M., Achtman M., Spratt B.G. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. USA 1998, 95:3140-3145.
46. Maynard-Smith J.M., Feil E., Smith N. Population structure and evolutionary dynamics of pathogenic bacteria. BioEssays 2000, 22:1115-1122.
47. Maynard-Smith J.M., Smith N.H., O'Rourke M., Spratt B.G. How clonal are bacteria?. Proc. Natl. Acad. Sci. USA 1993, 90:4384-4388.
48. Nataro J.P., Kaper J.B. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 1998, 11:142-201.
49. Navarro A., Eslava C., Hernandez U., Navarro-Henze J.L., Aviles M., Garcia-de la Torre G., Cravioto A. Antibody responses to Escherichia coli O157 and other lipopolysaccharides in healthy children and adults. Clin. Diagn. Lab. Immunol. 2003, 10:797-801.
50. Nicklasson M., Klena J., Rodas C., Bourgeois A.L., Tores O., et al. Enterotoxigenic Escherichia coli multilocus sequence types in Guatemala and Mexico. Emerg. Infect. Dis. 2010, 16:143-146.
51. Okeke I.N., Wallace-Gadsden F., Simons H.R., Matthews N., Labar A.S., Hwang J., Wain J. Multi-locus sequence typing of enteroaggregative Escherichia coli isolates from Nigerian children uncovers multiple lineages. PLoS One 2010, 5:e14093.
52. Orskov F., Orskov I. Serotyping of Escherichia coli. Methods Microbiol. 1984, 14:43-112.
53. Orskov F., Orskov I. Escherichia coli serotyping and disease in man and animals. Can. J. Microbiol. 1992, 38:699-704.
54. Paniagua G.L., Monroy E., García-González O., Alonso J., Negrete E., Vaca S. Two or more enteropathogens are associated with diarrhoea in Mexican children. Ann. Clin. Microbiol. Antimicrob. 2007, 6:17-24.
55. Parissi-Crivelli A., Parissi-Crivelli J., Girón J. Recognition of enteropathogenic Escherichia coli virulence determinants by human colostrum and serum antibodies. J. Clin. Microbiol. 2000, 38:2696-2700.
56. Partridge J.D., Scot C., Tang T., Poole R.K., Green J. Escherichia coli transcriptome dynamics during the transition from anaerobic to aerobic conditions. Journal of Biological Chemistry 2006, 281:2786-27815.
57. Peek A.S., Souza V., Eguiarte L.E., Gaut B.S. The interaction of protein structure, selection, and recombination on the evolutio of the type-1 fimbrial major subunit (fimA) from Escherichia coli. J. Mol. Evol. 2001, 52:193-204.
58. Perna N.T. Genomics of Escherichia and Shigella. Genomics of Foodborne Bacterial Pathogens 2011, 119-139. Springer, New York, USA. M. Wiedman, W. Zhang (Eds.).
59. Picard B., Garcia J.S., Gouriou S., Duriez P., Brahimi N., Bingen E., Elion J., Denamur E. The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect. Immun. 1999, 67:546-553.
60. Pond S.L., Frost S.D. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 2005, 21:2531-2533.
61. Power M.L., Littlefield-Wyer J., Gordon D.M., Veal D.A., Slade M.B. Phenotypic and genotypic characterization of encapsulated Escherichia coli isolated from blooms in two Australian lakes. Environ. Microbiol. 2005, 7:631-640.
62. Pritchard J.K., Stephens M., Donnelly P. Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.
63. Reid S.D., Herbelin C.J., Bumbaugh A.C., Selander R.K., Whittam T.S. Parallel evolution of virulence in pathogenic Escherichia coli. Nature 2000, 406:64-67.
64. Rozas J., Sanchez-DelBarrio J.C., Messeguer X., Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 2003, 19:2496-2497.
65. Sabarly V., Bouvet O., Glodt J., Clermont O., Skurnik D., Diancourt L., et al. The decoupling between genetic structure and metabolic phenotypes in Escherichia coli leads to continuous phenotypic diversity. J. Evol. Biol. 2011, 24:1559-1571.
66. Sandner L., Eguiarte L.E., Navarro A., Cravioto A., Souza V. The elements of the locus of enterocyte effacement in human and wild mammal isolates of Escherichia coli: evolution by assemblage or disruption?. Microbiology 2001, 147:3149-3158.
67. Savageau M.A. Escherichia coli habitats, cell types, and molecular mechanisms of gene control. Am. Nat. 1983, 122:732-744.
68. Selander R.K., Caugant D.A., Whittam T.S. Genetic structure and variation in natural populations of Escherichia coli. Escherichia coli and Salmonella typhimurirum: Cellular and Molecular Biology 1987, 1625-1648. ASM Press, Washington, DC. J.L. Ingraham, K.B. Low, B. Magasanik, M. Schaechter, H.E. Umbarger (Eds.).
69. Smith N.H., Dale J., Inwald J., Palmer S., Gordon S.V., Hewinson R.G., Maynard-Smith J. The population structure of Mycobacterium bovis in Great Britain: clonal expansion. Proc. Natl Acad. Sci. USA 2003, 100:5271-15275.
70. Souza V., Castillo A., Eguiarte L.E. The evolutionary ecology of Escherichia coli. Am. Sci. 2002, 90:332-341.
71. Souza V., Rocha M., Valera A., Eguiarte L.E. Genetic structure of natural populations of Escherichia coli in wild hosts on different continents. Appl. Environ. Microbiol. 1999, 65:3373-3385.
72. Souza V., Travisano M., Turner P., Eguiarte L.E. Does experimental evolution reflect patterns in natural populations? Comparison of E. coli strains from long-term studies to those from wild isolates. Antoine van Leeuwenhoek. 2002, 81:143-153.
73. Spratt B., Hanage W., Feil E. The relative contributions of recombination and point mutation to the diversification of bacterial clones. Curr. Opin. Microbiol. 2001, 4:602-606.
74. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
75. Suerbaum S., Smith J.M., Bapumia K., Morelli G., Smith N.H., Kunstmann E., Dyrek I., Achtman M. Free recombination within Helicobacter pylori. Proc. Natl. Acad. Sci. USA 1998, 95:12619-12624.
76. Tartof S.Y., Solberg O.D., Manges A.R., Riley L.W. Analysis of a uropathogenic Escherichia coli clonal group by multilocus sequence typing. J. Clin. Microbiol. 2005, 43:5860-5864.
77. Tenaillon O., Skurnik D., Picard B., Denamur E. The population genetics of commensal Escherichia coli. Nat. Rev. Microbiol. 2010, 8:207-217.
78. Thompson J., Higgins D., Gibson T. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 1994, 22:4673-4680.
79. Touchon M., Hoede C., Tenaillon O., Barbe V., Baeriswyl S., et al. Organised genome dynamics in Escherichia coli species results in highly diverse adaptive paths. PLoS Genetics 2009, 5:e1000344.
80. Turner S.M., Chaudhuri R.R., Jiang Z.D., DuPont H., Gyles C., et al. Phylogenetic comparisons reveal multiple acquisitions of the toxin genes by enterotoxigenic Escherichia coli strains of different evolutionary lineages. J. Clin. Microbiol. 2006, 44:4528-4536.
81. van Elsas J.D., Semenov A.V., Costa R., Trevors J.T. Survival of Escherichia coli in the environment: fundamental and public health aspects. ISME J. 2011, 5:173-183.
82. Vos M., Didelot X. A comparison of homologous recombination rates in bacteria and archaea. ISME J. 2009, 3:199-208.
83. Walk S.T., Alm E.W., Calhoun L.M., Mladonicky J.M., Whittam T.S. Genetic diversity and population structure of Escherichia coli isolated from freshwater beaches. Environ. Microbiol. 2007, 9:2274-2288.
84. Watanabe H., Wada A., Inagaki Y., Itoh K., Tamura K. Outbreaks of enterohaemorrhagic Escherichia coli O157:H7 infection by two different genotype strains in Japan, 1996. Lancet 1996, 348:831-832.
85. White A.P., Sibley K.A., Sibley C.D., Wasmuth J.D., Schaefer R., Surette M.G., Edge T.A., Neumann N.F. Intergenic sequence comparison of Escherichia coli isolates reveals lifestyle adaptations but not host specificity. Appl. Environ. Microbiol. 2011, 77:7620-7632.
86. Whitfield C. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu. Rev. Biochem. 2006, 75:39-68.
87. Whittam T.S., Ochman H., Selander R.K. Geographic components of linkage disequilibrium in natural populations of Escherichia coli. Mol. Biol. Evol. 1983, 1:67-83.
88. Wirth T., Falush D., Lan R., Colles F., Mensa P., Wieler L., Karch H., Reeves P., Maiden M., Ochman H., Achtman M. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol. Microbiol. 2006, 60:1136-1151.