The decoupling between genetic structure and metabolic phenotypes in Escherichia coli leads to continuous phenotypic diversity

Journal of Evolutionary Biology

Volumn 24, Issue 7, 2011, Pages 1559-1571

  Sabarly, V ^a,b,c   Bouvet, O ^b   Glodt, J ^b   Clermont, O ^b   Skurnik, D ^b   Diancourt, L ^d   De Vienne, D ^c   Denamur, E ^b   Dillmann, C ^c  

^a INRA Institut National de la Recherche Agronomique   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d INSTITUT PASTEUR   (France)

Author keywords

Carbon source; E. coli; Genetic distance; Genetic group; Lifestyle; Metabolic pathway; Natural isolate; Phenotypic distance

Indexed keywords

COLIFORM BACTERIUM; GENETIC STRUCTURE; GROWTH RESPONSE; LIFESTYLE; PATHOGENICITY; PHENOTYPE; PHYLOGENY;

ESCHERICHIA; ESCHERICHIA COLI; PROKARYOTA; SHIGELLA;

EID: 79959326367     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2011.02287.x     Document Type: Article

References (71)

1. Baldwin, A., Loughlin, M., Caubilla-Barron, J., Kucerova, E., Manning, G., Dowson, C. et al. 2009. Multilocus sequence typing of Cronobacter sakazakii and Cronobacter malonaticus reveals stable clonal structures with clinical significance which do not correlate with biotypes. BMC Microbiol. 9: 223.
2. Benjamini, Y. & Hochberg, Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57: 289-300.
3. Bernier-Febreau, C., du Merle, L., Turlin, E., Labas, V., Ordonez, J., Gilles, A. et al. 2004. Use of deoxyribose by intestinal and extraintestinal pathogenic Escherichia coli strains: a metabolic adaptation involved in competitiveness. Infect. Immun. 72: 6151-6156.
4. Bidet, P., Mahjoub-Messai, F., Blanco, J., Blanco, J., Dehem, M., Aujard, Y. et al. 2007. Combined multilocus sequence typing and O serogrouping distinguishes Escherichia coli subtypes associated with infant urosepsis and/or meningitis. J. Infect. Dis. 196: 297-303.
5. Burstin, J. & Charcosset, A. 1997. Relationship between phenotypic and marker distances: theoretical and experimental investigations. Heredity 79: 477-483.
6. Chang, D., Smalley, D.J., Tucker, D.L., Leatham, M.P., Norris, W.E., Stevenson, S.J. et al. 2004. Carbon nutrition of Escherichia coli in the mouse intestine. Proc. Natl Acad. Sci. USA 101: 7427-7432.
7. Clermont, O., Bonacorsi, S. & Bingen, E. 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl. Environ. Microbiol. 66: 4555-4558.
8. Clermont, O., Olier, M., Hoede, C., Diancourt, L., Brisse, S., Keroudean, M. et al. 2011. Animal and human pathogenic Escherichia coli strains share common genetic backgrounds. Infect. Genet. Evol. 11: 654-662.
9. Cooper, T.F., Rozen, D.E. & Lenski, R.E. 2003. Parallel changes in gene expression after 20, 000 generations of evolution in Escherichia coli. Proc. Natl Acad. Sci. USA 100: 1072-1077.
10. Dekel, E. & Alon, U. 2005. Optimality and evolutionary tuning of the expression level of a protein. Nature 436: 588-592.
11. Dray, S. & Dufour, A.B. 2007. The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22: 1-20.
12. Durot, M., Bourguignon, P.Y. & Schachter, V. 2009. Genome-scale models of bacterial metabolism: reconstruction and application. FEMS Microbiol. Rev. 33: 164-190.
13. Escobar-Páramo, P., Giudicelli, C., Parsot, C. & Denamur, E. 2003. The evolutionary history of Shigella and enteroinvasive Escherichia coli revised. J. Mol. Evol. 57: 140-148.
14. Escobar-Páramo, P., Clermont, O., Blanc-Potard, A., Bui, H., Le Bouguénec, C. & Denamur, E. 2004a. A specific genetic background is required for acquisition and expression of virulence factors in Escherichia coli. Mol. Biol. Evol. 21: 1085-1094.
15. Escobar-Páramo, P., Grenet, K., Le Menac'h, A., Rode, L., Salgado, E., Amorin, C. et al. 2004b. Large-scale population structure of human commensal Escherichia coli isolates. Appl. Environ. Microbiol. 70: 5698-5700.
16. Escobar-Páramo, P., Le Menac'h, A., Le Gall, T., Amorin, C., Gouriou, S., Picard, B. et al. 2006. Identification of forces shaping the commensal Escherichia coli genetic structure by comparing animal and human isolates. Environ. Microbiol. 8: 1975-1984.
17. Exley, R.M., Goodwin, L., Mowe, E., Shaw, J., Smith, H., Read, R.C. et al. 2005. Neisseria meningitidis lactate permease is required for nasopharyngeal colonization. Infect. Immun. 73: 5762-5766.
18. Fabich, A.J., Jones, S.A., Chowdhury, F.Z., Cernosek, A., Anderson, A., Smalley, D. et al. 2008. Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine. Infect. Immun. 76: 1143-1152.
19. Feist, A.M., Henry, C.S., Reed, J.L., Krummenacker, M., Joyce, A.R., Karp, P.D. et al. 2007. A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information. Mol. Syst. Biol. 3: 121.
20. Fontaneto, D., Herniou, E.A., Boschetti, C., Caprioli, M., Melone, G., Ricci, C. et al. 2007. Independently evolving species in asexual bdelloid rotifers. PLoS Biol. 5: e87.
21. Fox, J. & Weisberg, S. 2010. car: Companion to Applied Regression. See.
22. Fraley, C. & Raftery, A.E. 2002. Model-based clustering, discriminant analysis and density estimation. J. Am. Stat. Assoc. 97: 611-631.
23. Fraley, C. & Raftery, A.E. 2006. MCLUST version 3 for R: normal mixture modeling and model-based clustering. See.
24. Freter, R. 1983. Mechanisms that control the microflora in the large intestine. In: Human Intestinal Microflora in Health and Disease (D.J. Hentges, ed.), pp. 33-54. Academic Press, Inc., New York, NY.
25. Gordon, D.M. & Cowling, A. 2003. The distribution and genetic structure of Escherichia coli in Australian vertebrates: host and geographic effects. Microbiology 149: 3575-3586.
26. Guindon, S. & Gascuel, O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52: 696-704.
27. Guinebretière, M., Thompson, F.L., Sorokin, A., Normand, P., Dawyndt, P., Ehling-Schulz, M. et al. 2008. Ecological diversification in the Bacillus cereus group. Environ. Microbiol. 10: 851-865.
28. Guzmán, M.C., de los Angeles Bistoni, M., Tamagnini, L.M. & González, R.D. 2004. Recovery of Escherichia coli in fresh water fish, Jenynsia multidentata and Bryconamericus iheringi. Water Res. 38: 2368-2374.
29. Harder, W. & Dijkhuizen, L. 1982. Strategies of mixed substrate utilization in microorganisms. Philos. Trans. R. Soc. Lond. B Biol. Sci. 297: 459-480.
30. Hartl, D.L. & Dykhuizen, D.E. 1984. The population genetics of Escherichia coli. Annu. Rev. Genet. 18: 31-68.
31. Herring, C.D., Raghunathan, A., Honisch, C., Patel, T., Applebee, M.K., Joyce, A.R. et al. 2006. Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nat. Genet. 38: 1406-1412.
32. Herzer, P.J., Inouye, S., Inouye, M. & Whittam, T.S. 1990. Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J. Bacteriol. 172: 6175-6181.
33. Hobman, J.L., Penn, C.W. & Pallen, M.J. 2007. Laboratory strains of Escherichia coli: model citizens or deceitful delinquents growing old disgracefully? Mol. Microbiol. 64: 881-885.
34. Iyer, R. & Camilli, A. 2007. Sucrose metabolism contributes to in vivo fitness of Streptococcus pneumoniae. Mol. Microbiol. 66: 1-13.
35. Jaureguy, F., Landraud, L., Passet, V., Diancourt, L., Frapy, E., Guigon, G. et al. 2008. Phylogenetic and genomic diversity of human bacteremic Escherichia coli strains. BMC Genomics 9: 560.
36. Johnson, R., Colwell, R.R., Sakazaki, R. & Tamura, K. 1975. Numerical taxonomy study of the Enterobacteriaceae. Int. J. Syst. Bacteriol. 25: 12-37.
37. Kaper, J.B., Nataro, J.P. & Mobley, H.L. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2: 123-140.
38. Le Gall, T., Darlu, P., Escobar-Páramo, P., Picard, B. & Denamur, E. 2005. Selection-driven transcriptome polymorphism in Escherichia coli/Shigella species. Genome Res. 15: 260-268.
39. Lecointre, G., Rachdi, L., Darlu, P. & Denamur, E. 1998. Escherichia coli molecular phylogeny using the incongruence length difference test. Mol. Biol. Evol. 15: 1685-1695.
40. Lendenmann, U., Snozzi, M. & Egli, T. 1996. Kinetics of the simultaneous utilization of sugar mixtures by Escherichia coli in continuous culture. Appl. Environ. Microbiol. 62: 1493-1499.
41. MacLean, C.R. & Bell, G. 2002. Experimental adaptive radiation in Pseudomonas. Am. Nat. 160: 569-581.
42. MacLean, C.R. & Bell, G. 2003. Divergent evolution during an experimental adaptive radiation. Proc. Biol. Sci. 270: 1645-1650.
43. MacLean, C.R., Bell, G. & Rainey, P.B. 2004. The evolution of a pleiotropic fitness tradeoff in Pseudomonas fluorescens. Proc. Natl Acad. Sci. USA 101: 8072-8077.
44. Marshall, B., Petrowski, D. & Levy, S.B. 1990. Inter- and intraspecies spread of Escherichia coli in a farm environment in the absence of antibiotic usage. Proc. Natl Acad. Sci. USA 87: 6609-6613.
45. Martinez-Jéhanne, V., du Merle, L., Bernier-Fébreau, C., Usein, C., Gassama-Sow, A., Wane, A. et al. 2009. Role of deoxyribose catabolism in colonization of the murine intestine by pathogenic Escherichia coli strains. Infect. Immun. 77: 1442-1450.
46. Matias Rodrigues, J.F. & Wagner, A. 2009. Evolutionary plasticity and innovations in complex metabolic reaction networks. PLoS Comput. Biol. 5: e1000613.
47. Morandi, S., Brasca, M., Lodi, R., Brusetti, L., Andrighetto, C. & Lombardi, A. 2010. Biochemical profiles, restriction fragment length polymorphism (RFLP), random amplified polymorphic DNA (RAPD) and multilocus variable number tandem repeat analysis (MLVA) for typing Staphylococcus aureus isolated from dairy products. Res. Vet. Sci. 88: 427-435.
48. Moritz, R.L. & Welch, R.A. 2006. The Escherichia coli argW-dsdCXA genetic island is highly variable, and E. coli K1 strains commonly possess two copies of dsdCXA. J. Clin. Microbiol. 44: 4038-4048.
49. Mukherjee, A., Mammel, M.K., LeClerc, J.E. & Cebula, T.A. 2008. Altered utilization of N-acetyl-d-galactosamine by Escherichia coli O157:H7 from the 2006 spinach outbreak. J. Bacteriol. 190: 1710-1717.
50. Narang, A., Konopka, A. & Ramkrishna, D. 1997. New patterns of mixed-substrate utilization during batch growth of Escherichia coli K12. Biotechnol. Bioeng. 55: 747-757.
51. Ochman, H., Lawrence, J.G. & Groisman, E.A. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299-304.
52. Paradis, E., Claude, J. & Strimmer, K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289-290.
53. Patel, P.H. & Loeb, L.A. 2000. DNA polymerase active site is highly mutable: evolutionary consequences. Proc. Natl Acad. Sci. USA 97: 5095-5100.
54. Picard, B., Garcia, J.S., Gouriou, S., Duriez, P., Brahimi, N., Bingen, E. et al. 1999. The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect. Immun. 67: 546-553.
55. Pupo, G.M., Lan, R. & Reeves, P.R. 2000. Multiple independent origins of Shigella clones of Escherichia coli and convergent evolution of many of their characteristics. Proc. Natl Acad. Sci. USA 97: 10567-10572.
56. R Development Core Team. 2009. R: A Language and Environment for Statistical Computing. Vienna, Austria. See.
57. Rasko, D.A., Rosovitz, M.J., Myers, G.S.A., Mongodin, E.F., Fricke, W.F., Gajer, P. et al. 2008. The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J. Bacteriol. 190: 6881-6893.
58. Rio-Rodriguez, R.E., Inglis, V. & Millar, S.D. 1997. Survival of Escherichia coli in the intestine of fish. Aquac. Res. 28: 257-264.
59. Roldán-Ruiz, I., van Euwijk, F., Gilliland, T.J., Dubreuil, P., Dillmann, C., Lallemand, J. et al. 2001. A comparative study of molecular and morphological methods of describing relationships between perennial ryegrass (Lolium perenne L.) varieties. Theor. Appl. Genet. 103: 1138-1150.
60. Savageau, M.A. 1983. Escherichia coli habitats, cell types, and molecular mechanisms of gene control. Am. Nat. 122: 732-744.
61. Skurnik, D., Ruimy, R., Andremont, A., Amorin, C., Rouquet, P., Picard, B. et al. 2006. Effect of human vicinity on antimicrobial resistance and integrons in animal faecal Escherichia coli. J. Antimicrob. Chemother. 57: 1215-1219.
62. Sneath, P.H.A., Stevens, M. & Sackin, M.J. 1981. Numerical taxonomy of Pseudomonas based on published records of substrate utilization. Antonie Van Leeuwenhoek 47: 423-448.
63. Spor, A., Nidelet, T., Simon, J., Bourgais, A., de Vienne, D. & Sicard, D. 2009. Niche-driven evolution of metabolic and life-history strategies in natural and domesticated populations of Saccharomyces cerevisiae. BMC Evol. Biol. 9: 296.
64. Stackebrandt, E., Frederiksen, W., Garrity, G.M., Grimont, P.A.D., Kämpfer, P., Maiden, M.C.J. et al. 2002. Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int. J. Syst. Evol. Microbiol. 52: 1043-1047.
65. Strimmer, K. 2009. fdrtool: estimation and control of (local) false discovery rates. See.
66. Tenaillon, O., Skurnik, D., Picard, B. & Denamur, E. 2010. The population genetics of commensal Escherichia coli. Nat. Rev. Microbiol. 8: 207-217.
67. Touchon, M., Hoede, C., Tenaillon, O., Barbe, V., Baeriswyl, S., Bidet, P. et al. 2009. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet. 5: e1000344.
68. Venail, P.A., MacLean, R.C., Bouvier, T., Brockhurst, M.A., Hochberg, M.E. & Mouquet, N. 2008. Diversity and productivity peak at intermediate dispersal rate in evolving metacommunities. Nature 452: 210-214.
69. Vieira, G., Sabarly, V., Bourguignon, P., Durot, M., Le Fèvre, F., Mornico, D. et al. 2011. Core and panmetabolism in Escherichia coli. J. Bacteriol. 193: 1461-1472.
70. Walk, S.T., Alm, E.W., Gordon, D.M., Ram, J.L., Toranzos, G.A., Tiedje, J.M. et al. 2009. Cryptic lineages of the genus Escherichia. Appl. Environ. Microbiol. 75: 6534-6544.
71. Wayne, L., Brenner, D., Colwell, R., Grimont, P., Kandler, O., Krichevsky, M. et al. 1987. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int. J. Syst. Bacteriol. 37: 463-464.