The GimA locus of extraintestinal pathogenic E. coli: Does reductive evolution correlate with habitat and pathotype?

PLoS ONE

Volumn 5, Issue 5, 2010, Pages

  Homeier, Timo ^a,b   Semmler, Torsten ^a   Wieler, Lothar H ^a   Ewers, Christa ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI PROTEIN; INVASION OF BRAIN ENDOTHELIUM PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR; IBE10 PROTEIN, E COLI; MEMBRANE PROTEIN;

ARTICLE; AVIAN PATHOGENIC ESCHERICHIA COLI; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATION; CONTROLLED STUDY; DNA DNA HYBRIDIZATION; EVOLUTIONARY ADAPTATION; FECES MICROFLORA; GENE FUNCTION; GENE INSERTION; GENE LOCATION; GENE LOCUS; GENE REARRANGEMENT; GENETIC VARIABILITY; GENOME ANALYSIS; GENOMIC ISLAND; HABITAT SELECTION; MOLECULAR PHYLOGENY; MULTILOCUS SEQUENCE TYPING; NEWBORN MENINGITIC ESCHERICHIA COLI; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENIC ESCHERICHIA COLI; PATHOGENICITY ISLAND; PATHOTYPE; PHENOTYPE; POLYMERASE CHAIN REACTION; SEPTICEMIA ASSOCIATED ESCHERICHIA COLI; SEQUENCE ANALYSIS; SPECIES HABITAT; STRAIN DIFFERENCE; STRAIN IDENTIFICATION; UROPATHOGENIC ESCHERICHIA COLI; WILD TYPE; ANIMAL; BACTERIAL GENE; BINDING SITE; CLASSIFICATION; DNA SEQUENCE; ECOSYSTEM; ESCHERICHIA COLI; GENETICS; HUMAN; INTESTINE; MICROBIOLOGY; MOLECULAR EVOLUTION; MUTATION; PATHOGENICITY; PHYLOGENY;

ANIMALIA; AVES;

ANIMALS; BASE SEQUENCE; BINDING SITES; ECOSYSTEM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; EVOLUTION, MOLECULAR; GENES, BACTERIAL; GENETIC LOCI; HUMANS; INTESTINES; MEMBRANE PROTEINS; MUTATION; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

EID: 77956272810     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010877     Document Type: Article

References (69)

1. Kaper JB, Nataro JP, Mobley HL (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2: 123-140.
2. Gross WB (1994) Diseases due to Escherichia coli in poultry. In: Gyles CL, ed. Escherichia coli in domestic animals and humans. Wallingford, UK: CAB International: Wallingford, UK. pp 237-259.
3. Russo TA, Johnson JR (2000) Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli: ExPEC. J Infect Dis 181: 1753-1754.
4. Johnson JR, Russo TA (2002) Extraintestinal pathogenic Escherichia coli: ''the other bad E coli''. J Lab Clin Med 139: 155-162.
5. Bonacorsi S, Bingen E (2005) Molecular epidemiology of Escherichia coli causing neonatal meningitis. Int J Med Microbiol 295: 373-381.
6. Gross RJ, Ward LR, Threlfall EJ, Cheasty T, Rowe B (1983) Drug resistance among Escherichia coli strains isolated from cerebrospinal fluid. J Hyg (Lond) 90: 195-198.
7. Threlfall EJ, Cheasty T, Graham A, Rowe B (1997) Antibiotic resistance in Escherichia coli isolated from blood and cerebrospinal fluid: a 6-year study of isolates from patients in England and Wales. Int J Antimicrob Agents 9: 201-205.
8. Kim KS (2003) Pathogenesis of bacterial meningitis: from bacteraemia to neuronal injury. Nat Rev Neurosci 4: 376-385.
9. Leib SL, Tauber MG (1999) Pathogenesis of bacterial meningitis. Infect Dis Clin N Am 13: 527-548.
10. Hoffman JA, Badger JL, Zhang Y, Huang SH, Kim KS (2000) Escherichia coli K1 aslA contributes to invasion of brain microvascular endothelial cells in vitro and in vivo. Infect Immun 68: 5062-5067.
11. Huang SH, Wan ZS, Chen YH, Jong AY, Kim KS (2001) Further characterization of Escherichia coli brain microvascular endothelial cell invasion gene ibeA by deletion, complementation, and protein expression. J Infect Dis 183: 1071-1078.
12. Huang SH, Wass C, Fu Q, Prasadarao NV, Stins M, et al. (1995) Escherichia coli invasion of brain microvascular endothelial cells in vitro and in vivo: molecular cloning and characterization of invasion gene ibe10. Infect Immun 63: 4470-4475.
13. Huang SH, Chen YH, Fu Q, Stins M, Wang Y, et al. (1999) Identification and characterization of an Escherichia coli invasion gene locus, ibeB, required for penetration of brain microvascular endothelial cells. Infect Immun 67: 2103-2109.
14. Wang Y, Huang SH, Wass CA, Stins MF, Kim KS (1999) The gene locus yijP contributes to Escherichia coli K1 invasion of brain microvascular endothelial cells. Infect Immun 67: 4751-4756.
15. Prasadarao NV, Wass CA, Weiser JN, Stins MF, Huang SH, et al. (1996) Outer membrane protein A of Escherichia coli contributes to invasion of brain microvascular endothelial cells. Infect Immun 64: 146-153.
16. Kim KS (2002) Strategy of Escherichia coli for Crossing the Blood-Brain Barrier. J Infect Dis 186: S220-S224.
17. Germon P, Chen YH, He L, Blanco JE, Bree A, et al. (2005) ibeA, a virulence factor of avian pathogenic Escherichia coli. Microbiology 151: 1179-1186.
18. Huang SH, Chen YH, Kong G, Chen SH, Besemer J, et al. (2001) A novel genetic island of meningitic Escherichia coli K1 containing the ibeA invasion gene (GimA): functional annotation and carbon-source-regulated invasion of human brain microvascular endothelial cells. Funct Integr Genomics 1: 312-322.
19. Wang D, Ding X, Rather PN (2001) Indole Can Act as an Extracellular Signal in Escherichia coli. J Bacteriol 183: 4210-4216.
20. Ewers C, Li G, Wilking H, Kiessling S, Alt K, et al. (2007) Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they? Int J Med Microbiol 297: 163-176.
21. Moulin-Schouleur M, Reperant M, Laurent S, Bree A, Mignon-Grasteau S, et al. (2007) Extraintestinal pathogenic Escherichia coli strains of avian and humanorigin: link between phylogenetic relationships and common virulence patterns. J Clin Microbiol 45: 3366-3376.
22. Johnson TJ, Wannemuehler Y, Johnson SJ, Stell AL, Doetkott C, et al. (2008) Comparison of Extraintestinal Pathogenic Escherichia coli Strains from Human and Avian Sources Reveals a Mixed Subset Representing Potential Zoonotic Pathogens. Appl Environ Microbiol 74: 7043-7050.
23. Gordon D, Clermont O, Tolley H, Denamur E (2008) Assigning Escherichia coli strains to phylogenetic groups: multi-locus sequence typing versus the PCR triplex method. Environ Microbiol 10: 2484-2496.
24. Ochman H, Selander RK (1984) Standard reference strains of Escherichia coli from natural populations. J Bacteriol 157: 690-693.
25. Wirth T, Falush D, Lan R, Colles F, Mensa P, et al. (2006) Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60: 1136-1151.
26. Ewers C, Grobbel M, Stamm I, Kopp PA, Diehl I, et al. (2010) Emergence of human pandemic O25:H4-ST131 CTX-M-15 extended-spectrum-{beta}-lactamase-producing Escherichia coli among companion animals. J Antimicrob Chemother 65: 651-660.
27. Mordhorst IL, Claus H, Ewers C, Lappann M, Schoen C, et al. (2009) Oacetyltransferase gene neuO is segregated according to phylogenetic background and contributes to environmental desiccation resistance in Escherichia coli K1. Environ Microbiol 11: 3154-3165.
28. Sankar TS, Neelakanta G, Sangal V, Plum G, Achtman M, et al. (2009) Fate of the H-NS-Repressed bgl Operon in Evolution of Escherichia coli. PLoS Genet 5: e1000405.
29. Ewers C, Antao E-M, Diehl I, Philipp H-C, Wieler LH (2009) Intestine and Environment of the Chicken as Reservoirs for Extraintestinal Pathogenic Escherichia coli Strains with Zoonotic Potential. Appl Environ Microbiol 75: 184-192.
30. Welch RA, Burland V, Plunkett G, Redford P, Roesch P, et al. (2002) Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci USA 99: 17020-17024.
31. Chen SL, Hung C-S, Xu J, Reigstad CS, Magrini V, et al. (2006) Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: A comparative genomics approach. Proc Natl Acad Sci USA 103: 5977-5982.
32. Rasko DA, Rosovitz MJ, Myers GSA, Mongodin EF, Fricke WF, et al. (2008) The pangenome structure of Escherichia coli: Comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 190: 6881-6893.
33. Hochhut B, Wilde C, Balling G, Middendorf B, Dobrindt U, et al. (2006) Role of pathogenicity island-associated integrases in the genome plasticity of uropathogenic Escherichia coli strain 536. Mol Microbiol 61: 584-595.
34. Johnson TJ, Kariyawasam S, Wannemuehler Y, Mangiamele P, Johnson SJ, et al. (2007) The Genome Sequence of Avian Pathogenic Escherichia coli Strain O1:K1:H7 Shares Strong Similarities with Human Extraintestinal Pathogenic E. coli Genomes. J Bacteriol 189: 3228-3236.
35. Blattner FR, Plunkett G, III, Bloch CA, Perna NT, Burland V, et al. (1997) The Complete Genome Sequence of Escherichia coli K-12. Science 277: 1453-1462.
36. Ausubel FM (1999) Short Protocols in molecular biology; Ausubel FMB R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K, eds. New York, NY: John Wiley & Sons, Inc. pp 15.11-15.12.
37. Didelot X, Falush D (2007) Inference of bacterial microevolution using multilocus sequence data. Genetics 175: 1251-1266.
38. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Mol Biol Evol 24: 1596-1599.
39. Falush D, Wirth T, Linz B, Pritchard JK, Stephens M, et al. (2003) Traces of human migrations in Helicobacter pylori populations. Science 299: 1582-1585.
40. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567-1587.
41. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497.
42. Pond SL, Frost SD (2005) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21: 2531-2533.
43. Hughes AL, Nei M (1989) Nucleotide Substitution at Major HistocompatibilityComplex Class-Ii Loci - Evidence for Overdominant Selection. Proc Natl Acad Sci USA 86: 958-962.
44. Tanaka T, Nei M (1989) Positive darwinian selection observed at the variableregion genes of immunoglobulins. Mol Biol Evol 6: 447-459.
45. Mora A, Lopez C, Dabhi G, Blanco M, Blanco J, et al. (2009) Extraintestinal pathogenic Escherichia coli O1:K1:H7/NM from human and avian origin: detection of clonal groups B2 ST95 and D ST59 with different host distribution. BMC Microbiol 9: 132-143.
46. Culham DE, Wood JM (2000) An Escherichia coli reference collection group B2- and uropathogen-associated polymorphism in the rpoS-mutS region of the E. coli chromosome. J Bacteriol 182: 6272-6276.
47. Jores J, Rumer L, Kiessling S, Kaper JB, Wieler LH (2001) A novel locus of enterocyte effacement (LEE) pathogenicity island inserted at pheV in bovine Shiga toxin-producing Escherichia coli strain O103:H2. FEMS Microbiol Lett 204: 75-79.
48. Jores J, Rumer L, Wieler LH (2004) Impact of the locus of enterocyte effacement pathogenicity island on the evolution of pathogenic Escherichia coli. Int J Med Microbiol 294: 103-113.
49. Sandner L, Eguiarte LE, Navarro A, Cravioto A, Souza V (2001) The elements of the focus of enterocyte effacement in human and wild mammal isolates of Escherichia coli: evolution by assemblage or disruption? Microbiology-Sgm 147: 3149-3158.
50. Chongtrakool P, Ito T, Ma XX, Kondo Y, Trakulsomboon S, et al. (2006) Staphylococcal Cassette Chromosome mec (SCCmec) Typing of Methicillin- Resistant Staphylococcus aureus Strains Isolated in 11 Asian Countries: a Proposal for a New Nomenclature for SCCmec Elements. Antimicrob Agents Chemother 50: 1001-1012.
51. Coleman ML, Sullivan MB, Martiny AC, Steglich C, Barry K, et al. (2006) Genomic Islands and the Ecology and Evolution of Prochlorococcus. Science 311: 1768-1770.
52. Hacker J, Blum-Oehler G, Muhldorfer I, Tschape H (1997) Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol Microbiol 23: 1089-1097.
53. Hacker J, Kaper JB (2000) Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol 54: 641-679.
54. Zhang R, Zhang CT (2004) A systematic method to identify genomic islands and its applications in analyzing the genomes of Corynebacterium glutamicum and Vibriovulnificus CMCP6 chromosome I. Bioinformatics 20: 612-622.
55. Tartof SY, Solberg OD, Riley LW (2007) Genotypic analyses of uropathogenic Escherichia coli based on fimH single nucleotide polymorphisms (SNPs). J Med Microbiol 56: 1363-1369.
56. Weissman SJ, Chattopadhyay S, Aprikian P, Obata-Yasuoka M, Yarova-Yarovaya Y, et al. (2006) Clonal analysis reveals high rate of structural mutations in fimbrial adhesins of extraintestinal pathogenic Escherichia coli. Mol Microbiol 59: 975-988.
57. Antao E-M, Ewers C, Gürlebeck D, Preisinger R, Homeier T, et al. (2009) Signature-Tagged Mutagenesis in a Chicken Infection Model Leads to the Identification of a Novel Avian Pathogenic Escherichia coli Fimbrial Adhesin. PLoS ONE 4: e7796.
58. Touchon M, Hoede C, Tenaillon O, Barbe VR, Baeriswyl S, et al. (2009) Organised Genome Dynamics in the Escherichia coli Species Results in Highly Diverse Adaptive Paths. PLoS Genet 5: e1000344.
59. Clermont O, Bonacorsi S, Bingen E (2000) Rapid and Simple Determination of the Escherichia coli Phylogenetic Group. Appl Environ Microbiol 66: 4555-4558.
60. Dobrindt U, Hochhut B, Hentschel U, Hacker J (2004) Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol 2: 414-424.
61. Andersson SG, Kurland CG (1998) Reductive evolution of resident genomes. Trends Microbiol 6: 263-268.
62. Meseguer MA, Álvarez A, Rejas MT, Sánchez C, Pérez-Díaz JC, et al. (2003) Mycoplasma pneumoniae: a reduced-genome intracellular bacterial pathogen. Infect Genet Evol 3: 47-55.
63. Tamames J, Moya A, Valencia A (2007) Modular organization in the reductiveevolution of protein-protein interaction networks. Genome Biol 8: R94.
64. Oshima K, Kakizawa S, Nishigawa H, Jung HY, Wei W, et al. (2004) Reductive evolution suggested from the complete genome sequence of a plant-pathogenic phytoplasma. Nat Genet 36: 27-29.
65. Sokurenko EV, Hasty DL, Dykhuizen DE (1999) Pathoadaptive mutations: gene loss and variation in bacterial pathogens. Trends Microbiol 7: 191-195.
66. Zou YM, He L, Chi F, Jong A, Huang SH (2008) Involvement of Escherichia coli K1 ibeT in bacterial adhesion that is associated with the entry into human brain microvascular endothelial cells. Med Microbiol Immun 197: 337-344.
67. Cortes MAM, Gibon J, Chanteloup NK, Moulin-Schouleur M, Gilot P, et al. (2008) Inactivation of ibeA and ibeT Results in Decreased Expression of Type 1 Fimbriae in Extraintestinal Pathogenic Escherichia coli Strain BEN2908. Infect Immun 76: 4129-4136.
68. Chi F, Wang Y, Gallaher TK, Wu CH, Jong A, et al. (2009) Identification of IbeR as a Stationary-Phase Regulator in Meningitic Escherichia coli K1 that Carries a Loss-of-Function Mutation in rpoS. J Biomed Biotechnol vol.2009: Article ID 520283.
69. Hejnova J, Dobrindt U, Nemcova R, Rusniok C, Bomba A, et al. (2005) Characterization of the flexible genome complement of the commensal Escherichia coli strain A0 34/86 (O83: K24: H31). Microbiology 151: 385-398.