1887

Abstract

, the common inhabitant of the mammalian intestine, exhibits considerable intraspecies genomic variation, which has been suggested to reflect adaptation to different ecological niches. Also, regulatory trade-offs, e.g. between catabolic versatility and stress protection, are thought to result in significant physiological differences between strains. For these reasons, the relevance of experimental observations made for ‘domesticated’ strains with regard to the behaviour of this species in its natural environments is often questioned and doubts are frequently raised on the status of as a defined species. The variability of important (eco-)physiological functions, such as carbon substrate uptake and breakdown capabilities, as well as stress defence mechanisms, in the genomes of commensal and pathogenic strains were therefore investigated. Furthermore, (eco-)physiological properties of environmental strains were compared to standard laboratory strain K-12 MG1655. Catabolic, stress protection, and carbon- and energy source transport operons showed a very low intraspecies variability in 57 commensal and pathogenic . Environmental isolates adapted to glucose-limited growth in a similar way as MG1655, namely by increasing their catabolic flexibility and by inducing high-affinity substrate uptake systems. The results obtained indicate that significant (eco-)physiological properties are highly conserved in the natural population of . This questions the proposed dominant role of horizontal gene transfer for niche adaptation.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2006/002006-0
2007-07-01
2020-03-31
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/7/2052.html?itemId=/content/journal/micro/10.1099/mic.0.2006/002006-0&mimeType=html&fmt=ahah

References

  1. Ames G. F., Prody C., Kustu S.. 1984; Simple, rapid, and quantitative release of periplasmic proteins by chloroform. J Bacteriol160:1181–1183
    [Google Scholar]
  2. Anjum M. F., Lucchini S., Thompson A., Hinton J. C., Woodward M. J.. 2003; Comparative genomic indexing reveals the phylogenomics of Escherichia coli pathogens. Infect Immun71:4674–4683[CrossRef]
    [Google Scholar]
  3. Bergthorsson U., Ochman H.. 1998; Distribution of chromosome length variation in natural isolates of Escherichia coli. Mol Biol Evol15:6–16[CrossRef]
    [Google Scholar]
  4. Berlyn M. K.. 1998; Linkage map of Escherichia coli K-12, edition 10: the traditional map. Microbiol Mol Biol Rev62:814–984
    [Google Scholar]
  5. Bettelheim K. A.. 1992; The genus Escherichia . In The Prokaryotes pp2696–2736 Edited by Balows A., Dworkin M., Harder W., Schleifer K.-H., Trüper H. G.. New York: Springer Verlag;
    [Google Scholar]
  6. Beutin L., Montenegro M. A., Orskov I., Orskov F., Prada J., Zimmermann S., Stephan R.. 1989; Close association of verotoxin (Shiga-like toxin) production with enterohemolysin production in strains of Escherichia coli. J Clin Microbiol27:2559–2564
    [Google Scholar]
  7. Blattner F. R., Bloch C., Perna N., Burland V., Riley M., Collado-Vides J., Glasner J., Rode C., other authors Plunkett G. III. 1997; The complete genome sequence of Escherichia coli K-12. Science277:1453–1462[CrossRef]
    [Google Scholar]
  8. Blum G., Ott M., Lischewski A., Ritter A., Imrich H., Tschape H., Hacker J.. 1994; Excision of large DNA regions termed pathogenicity islands from tRNA-specific loci in the chromosome of an Escherichia coli wild-type pathogen. Infect Immun62:606–614
    [Google Scholar]
  9. Booth I. R., Cash P., O'Byrne C.. 2002; Sensing and adapting to acid stress. Antonie Van Leeuwenhoek81:33–42[CrossRef]
    [Google Scholar]
  10. Charbonnier Y., Gettler B., Bento M., Renzoni A., Vaudaux P., Schlegel W., Schrenzel J., Patrice François P.. 2005; A generic approach for the design of whole-genome oligoarrays, validated for genomotyping, deletion mapping and gene expression analysis on Staphylococcus aureus. BMC Genomics6:95[CrossRef]
    [Google Scholar]
  11. Chen G., Patten C. L., Schellhorn H. E.. 2004; Positive selection for loss of RpoS function in Escherichia coli. Mutat Res554:193–203[CrossRef]
    [Google Scholar]
  12. Clermont O., Bonacorsi S., Bingen E.. 2000; Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol66:4555–4558[CrossRef]
    [Google Scholar]
  13. Cooper V. S., Lenski R. E.. 2000; The population genetics of ecological specialization in evolving Escherichia coli populations. Nature407:736–739[CrossRef]
    [Google Scholar]
  14. Dagan T., William M.. 2006; The tree of one percent. Genome Biol7:118[CrossRef]
    [Google Scholar]
  15. Dobrindt U., Agerer F., Michaelis K., Janka A., Buchrieser C., Samuelson M., Svanborg C., Gottschalk G., Karch H., Hacker J.. 2003; Analysis of genome plasticity in pathogenic and commensal Escherichia coli isolates by use of DNA arrays. J Bacteriol185:1831–1840[CrossRef]
    [Google Scholar]
  16. Dobrindt U., Hochhut B., Hentschel U., Hacker J.. 2004; Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol2:414–424[CrossRef]
    [Google Scholar]
  17. Doolittle W. F.. 1999; Phylogenetic classification and the universal tree. Science284:2124–2129[CrossRef]
    [Google Scholar]
  18. Durso L. M., Smith D., Hutkins R. W.. 2004; Measurements of fitness and competition in commensal Escherichia coli and E. coli O157 : H7 strains. Appl Environ Microbiol70:6466–6472[CrossRef]
    [Google Scholar]
  19. Egli T.. 1995; The ecological and physiological significance of the growth of heterotrophic microorganisms with mixtures of substrates. Adv Microb Ecol14:305–386
    [Google Scholar]
  20. Eisenstark A., Calcutt M. J., Becker-Hapak M., Ivanova A.. 1996; Role of Escherichia coli rpoS and associated genes in defence against oxidative damage. Free Radic Biol Med21:975–993[CrossRef]
    [Google Scholar]
  21. Ferenci T.. 2001; Hungry bacteria – definition and properties of a nutritional state. Environ Microbiol3:605–611[CrossRef]
    [Google Scholar]
  22. Freter R., Brickner H., Fekete J., Vickerman M. M., Carey K. E.. 1983a; Survival and implantation of Escherichia coli in the intestinal tract. Infect Immun39:686–703
    [Google Scholar]
  23. Freter R., Brickner H., Botney M., Cleven D., Aranki A.. 1983b; Mechanisms that control bacterial populations in continuous-flow culture models of mouse large intestinal flora. Infect Immun39:676–685
    [Google Scholar]
  24. Gordon D. M., Riley M. A., Pinou T.. 1998; Temporal changes in the frequency of colicinogeny in Escherichia coli from house mice. Microbiology144:2233–2240[CrossRef]
    [Google Scholar]
  25. Hacker J., Kaper J. B.. 2000; Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol54:641–679[CrossRef]
    [Google Scholar]
  26. Hashimoto M., Ichimura T., Mizoguchi H., Tanaka K., Fujimitsu K., Keyamura K., Ote T., Yamakawa T., Yamazaki Y.. other authors 2005; Cell size and nucleoid organization of engineered Escherichia coli cells with a reduced genome. Mol Microbiol55:137–149
    [Google Scholar]
  27. Hengge-Aronis R.. others 1996; Regulation of gene expression during entry into stationary phase. In Escherichia coli and Salmonella: Cellular and Molecular Biology pp1497–1512 Edited by Neidhardt F. C.. Washington, DC: ASM Press;
    [Google Scholar]
  28. Holt J. G.. 1994; Bergey's Manual of Determinative Bacteriology Baltimore, USA: Williams & Wilkins;
    [Google Scholar]
  29. Ihssen J., Egli T.. 2004; Specific growth rate and not cell density controls the general stress response in Escherichia coli. Microbiology150:1637–1648[CrossRef]
    [Google Scholar]
  30. Ihssen J., Egli T.. 2005; Global physiological analysis of carbon- and energy-limited growing Escherichia coli confirms a high degree of catabolic flexibility and preparedness for mixed substrate utilization. Environ Microbiol7:1568–1581[CrossRef]
    [Google Scholar]
  31. Ishihama A.. 2000; Functional modulation of Escherichia coli RNA polymerase. Annu Rev Microbiol54:499–518[CrossRef]
    [Google Scholar]
  32. Kanehisa M., Goto S.. 2000; KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res28:27–30[CrossRef]
    [Google Scholar]
  33. Keseler I. M., Collado-Vides J., Gama-Castro S., Ingraham J., Paley S., Paulsen I. T., Peralta-Gil M., Karp P. D.. 2005; EcoCyc: a comprehensive database resource for Escherichia coli. Nucleic Acids Res33:D334–D337
    [Google Scholar]
  34. Kim C. C., Joyce E. A., Chan K., Falkow S.. 2002; Improved analytical methods for microarray-based genome-composition analysis. Genome Biol3:
    [Google Scholar]
  35. King T., Ishihama A., Kori A., Ferenci T.. 2004; A regulatory trade-off as a source of strain variation in the species Escherichia coli. J Bacteriol186:5614–5620[CrossRef]
    [Google Scholar]
  36. Kurland C. G.. 2005; What tangled web: barriers to rampant horizontal gene transfer. Bioessays27:741–747[CrossRef]
    [Google Scholar]
  37. Lan R., Reeves P. R.. 2000; Intraspecies variation in bacterial genomes: the need for a species genome concept. Trends Microbiol8:396–401[CrossRef]
    [Google Scholar]
  38. Lange R., Hengge-Aronis R.. 1994; The cellular concentration of the σ S subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation, and protein stability. Genes Dev8:1600–1612[CrossRef]
    [Google Scholar]
  39. Lawrence J. G.. 2001; Catalyzing bacterial speciation: correlating lateral transfer with genetic headroom. Syst Biol50:479–496[CrossRef]
    [Google Scholar]
  40. Lawrence J. G., Ochman H.. 1998; Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci U S A95:9413–9417[CrossRef]
    [Google Scholar]
  41. Lin E. C. C.. others 1996; Dissimilatory pathways for sugars, polyols and carboxylates. In Escherichia coli and Salmonella: Cellular and Molecular Biology pp307–342 Edited by Neidhardt F. C.. Washington, DC: ASM Press;
    [Google Scholar]
  42. Liu M., Durfee T., Cabrera J. E., Zhao K., Jin D. J., Blattner F. R.. 2005; Global transcriptional programs reveal a carbon source foraging strategy by Escherichia coli. J Biol Chem280:15921–15927[CrossRef]
    [Google Scholar]
  43. Loewen P. C., Hu B., Strutinsky J., Sparling R.. 1998; Regulation in the rpoS regulon of Escherichia coli. Can J Microbiol44:707–717[CrossRef]
    [Google Scholar]
  44. Macfarlane G. T., Macfarlane S.. 1997; Human colonic microbiota: ecology, physiology and metabolic potential of intestinal bacteria. Scand J Gastroenterol Suppl222:3–9
    [Google Scholar]
  45. Macfarlane G. T., Macfarlane S., Gibson G. R.. 1998; Validation of a three-stage compound continuous culture system for investigating the effect of retention time on the ecology and metabolism of bacteria in the human colon. Microb Ecol35:180–187[CrossRef]
    [Google Scholar]
  46. Manché K., Notley-McRobb L., Ferenci T.. 1999; Mutational adaptation of Escherichia coli to glucose limitation involves distinct evolutionary pathways in aerobic and oxygen-limited environments. Genetics153:5–12
    [Google Scholar]
  47. Mason T. G., Richardson G.. 1981; Escherichia coli and the human gut: some ecological considerations. J Appl Bacteriol51:1–16[CrossRef]
    [Google Scholar]
  48. Matin A.. 1991; The molecular basis of carbon-starvation-induced general resistance in Escherichia coli. Mol Microbiol5:3–10[CrossRef]
    [Google Scholar]
  49. Matin A. C.. 2004; Starvation, bacterial. In Desk Encyclopedia of Microbiology pp951–959 Edited by Schaechter M.. Amsterdam: Elsevier Academic Press;
    [Google Scholar]
  50. McFall E., Newman E. B.. others 1996; Amino acids as carbon sources. In Escherichia coli and Salmonella: Cellular and Molecular Biology pp307–342 Edited by Neidhardt F. C.. Washington, DC: ASM Press;
    [Google Scholar]
  51. Mikkola R., Kurland C. G.. 1992; Selection of laboratory wild-type phenotype from natural isolates of Escherichia coli in chemostats. Mol Biol Evol9:394–402
    [Google Scholar]
  52. Miller R. D., Hartl D. L.. 1986; Biotyping confirms a nearly clonal population structure in Escherichia coli. Evolution40:1–12[CrossRef]
    [Google Scholar]
  53. Munro P. M., Flatau G. N., Clement R. L., Gauthier M. J.. 1995; Influence of the RpoS (KatF) sigma factor on maintenance of viability and culturability of Escherichia coli and Salmonella typhimurium in seawater. Appl Environ Microbiol61:1853–1858
    [Google Scholar]
  54. Notley-McRobb L., Ferenci T.. 1999a; Adaptive mgl -regulatory mutations and genetic diversity evolving in glucose-limited Escherichia coli populations. Environ Microbiol1:33–43[CrossRef]
    [Google Scholar]
  55. Notley-McRobb L., Ferenci T.. 1999b; The generation of multiple coexisting mal -regulatory mutations through polygenic evolution in glucose-limited populations of Escherichia coli. Environ Microbiol1:45–52[CrossRef]
    [Google Scholar]
  56. Notley-McRobb L., King T., Ferenci T.. 2002; rpoS mutations and loss of general stress resistance in Escherichia coli populations as a consequence of conflict between competing stress responses. J Bacteriol184:806–811[CrossRef]
    [Google Scholar]
  57. Nowrouzian F. L., Adlerberth I., Wold A.. 2006; Enhanced persistence in the colonic microbiota of Escherichia coli strains belonging to phylogenetic group B2: role of virulence factors and adherence to colonic cells. Microbes Infect8:834–840[CrossRef]
    [Google Scholar]
  58. Nyström T.. 2004; Stationary-phase physiology. Annu Rev Microbiol58:161–181[CrossRef]
    [Google Scholar]
  59. Ochman H., Lawrence J. G., Groisman E. A.. 2000; Lateral gene transfer and the nature of bacterial innovation. Nature405:299–304[CrossRef]
    [Google Scholar]
  60. Ölschläger T., Schramm E., Braun V.. 1984; Cloning and expression of the activity and immunity genes of colicins B and M on ColBM plasmids. Mol Gen Genet196:482–487[CrossRef]
    [Google Scholar]
  61. Peekhaus N., Conway T.. 1998; What's for dinner?: Entner-Doudoroff metabolism in Escherichia coli. J Bacteriol180:3495–3502
    [Google Scholar]
  62. Perna N. T., Burland V., Mau B., Glasner J. D., Rose D. J., Mayhew G. F., Evans P. S., Gregor J., other authors Plunkett G. III. 2001; Genome sequence of enterohaemorrhagic Escherichia coli O157 : H7. Nature409:529–533[CrossRef]
    [Google Scholar]
  63. Philippe H., Douady C. J.. 2003; Horizontal gene transfer and phylogenetics. Curr Opin Microbiol6:498–505[CrossRef]
    [Google Scholar]
  64. Reeves P. R.. 1992; Variation in O-antigens, niche-specific selection and bacterial populations. FEMS Microbiol Lett79:509–516
    [Google Scholar]
  65. Savageau M. A.. 1983; Escherichia coli habitats, cell types and molecular mechanisms of gene control. Am Nat122:732–744[CrossRef]
    [Google Scholar]
  66. Schwyn B., Neilands J. B.. 1987; Universal chemical assay for the detection and determination of siderophores. Anal Biochem160:47–56[CrossRef]
    [Google Scholar]
  67. Selander R. K., Caugant D. A., Whittam T. S.. others 1996; Genetic structure and variation in natural populations of Escherichia coli . In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology pp1625–1648 Edited by Neidhardt F. C.. Washington, DC: ASM Press;
    [Google Scholar]
  68. Senn H., Lendenmann U., Snozzi M., Hamer G., Egli T.. 1994; The growth of Escherichia coli in glucose-limited chemostat cultures: a re-examination of the kinetics. Biochim Biophys Acta1201:424–436[CrossRef]
    [Google Scholar]
  69. Shehata T. E., Marr A. G.. 1971; Effect of nutrient concentration on the growth of Escherichia coli. J Bacteriol107:210–216
    [Google Scholar]
  70. Smith H. W., Huggins M. B.. 1978; The effect of plasmid-determined and other characteristics on the survival of Escherichia coli in the alimentary tract of two human beings. J Gen Microbiol109:375–379[CrossRef]
    [Google Scholar]
  71. Smith H. W., Parsell Z.. 1975; Transmissible substrate-utilizing ability in enterobacteria. J Gen Microbiol87:129–140[CrossRef]
    [Google Scholar]
  72. Soupene E., Plumbridge J., Stewart V., Bertenthal D., Lee H., Prasad G., Paliy O., Charernnoppakul P., Kustu S., van Heeswijk W. C.. 2003; Physiological studies of Escherichia coli strain MG1655: growth defects and apparent cross-regulation of gene expression. J Bacteriol185:5611–5626[CrossRef]
    [Google Scholar]
  73. Stoebel D. M.. 2004; Lack of evidence for horizontal transfer of the lac operon into Escherichia coli. Mol Biol Evol22:683–690[CrossRef]
    [Google Scholar]
  74. Visick J. E., Clarke S.. 1997; RpoS- and OxyR-independent induction of HPI catalase at stationary phase in Escherichia coli and identification of rpoS mutations in common laboratory strains. J Bacteriol179:4158–4163
    [Google Scholar]
  75. Waterman S. R., Small P. L.. 1996; Characterization of the acid resistance phenotype and rpoS alleles of shiga-like toxin-producing Escherichia coli. Infect Immun64:2808–2811
    [Google Scholar]
  76. Welch R. A., Burland V., Redford P., Roesch P., Rasko D., Buckles E. L., Liou S. R., Boutin A., Plunkett G. III. other authors 2002; Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A99:17020–17024[CrossRef]
    [Google Scholar]
  77. Wick L. M., Egli T.. 2004; Molecular components of physiological stress responses in Escherichia coli. Adv Biochem Eng Biotechnol89:1–45
    [Google Scholar]
  78. Wick L. M., Quadroni M., Egli T.. 2001; Short- and long-term changes in proteome composition and kinetic properties in a culture of Escherichia coli during transition from glucose-excess to glucose-limited growth conditions in continuous culture and vice versa. Environ Microbiol3:588–599[CrossRef]
    [Google Scholar]
  79. Wick L. M., Weilenmann H., Egli T.. 2002; The apparent clock-like evolution of Escherichia coli in glucose-limited chemostats is reproducible at large but not at small population sizes and can be explained with Monod kinetics. Microbiology148:2889–2902
    [Google Scholar]
  80. Wick L. M., Qi W., Lacher D. W., Whittam T. S.. 2005; Evolution of genomic content in the stepwise emergence of Escherichia coli O157 : H7. J Bacteriol187:1783–1791[CrossRef]
    [Google Scholar]
  81. Zinser E. R., Kolter R.. 1999; Mutations enhancing amino acid catabolism confer a growth advantage in stationary phase. J Bacteriol181:5800–5807
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2006/002006-0
Loading
/content/journal/micro/10.1099/mic.0.2006/002006-0
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error