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PMID: 16585510 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 103 ·No. 15 ·2006-04-11 ·Pages 5977-82

Chen SL, Hung CS, Xu J, Reigstad CS, Magrini V, Sabo A, Blasiar D, Bieri T, Meyer RR, Ozersky P, Armstrong JR, Fulton RS, Latreille JP, Spieth J, Hooton TM, Mardis ER, Hultgren SJ, Gordon JI

Abstract

Escherichia coli is a model laboratory bacterium, a species that is widely distributed in the environment, as well as a mutualist and pathogen in its human hosts. As such, E. coli represents an attractive organism to study how environment impacts microbial genome structure and function. Uropathogenic E. coli (UPEC) must adapt to life in several microbial communities in the human body, and has a complex life cycle in the bladder when it causes acute or recurrent urinary tract infection (UTI). Several studies designed to identify virulence factors have focused on genes that are uniquely represented in UPEC strains, whereas the role of genes that are common to all E. coli has received much less attention. Here we describe the complete 5,065,741-bp genome sequence of a UPEC strain recovered from a patient with an acute bladder infection and compare it with six other finished E. coli genome sequences. We searched 3,470 ortholog sets for genes that are under positive selection only in UPEC strains. Our maximum likelihood-based analysis yielded 29 genes involved in various aspects of cell surface structure, DNA metabolism, nutrient acquisition, and UTI. These results were validated by resequencing a subset of the 29 genes in a panel of 50 urinary, periurethral, and rectal E. coli isolates from patients with UTI. These studies outline a computational approach that may be broadly applicable for studying strain-specific adaptation and pathogenesis in other bacteria.

MeSH Terms
Chromosomes, Bacterial Escherichia coli/classification,genetics,pathogenicity Escherichia coli Infections/genetics Genome, Bacterial Humans Models, Genetic Molecular Sequence Data Phylogeny Recombination, Genetic Selection, Genetic Urinary Tract Infections/microbiology
Authors & Affiliations
18 authors, click to expand affiliations / ORCID
Chen Swaine L
Center for Genome Sciences, Washington University School of Medicine, St. Louis, MO 63110, USA.
Hung Chia-Seui
Xu Jian
Reigstad Christopher S
Magrini Vincent
Sabo Aniko
Blasiar Darin
Bieri Tamberlyn
Meyer Rekha R
Ozersky Philip
Armstrong Jon R
Fulton Robert S
Latreille J Phillip
Spieth John
Hooton Thomas M
Mardis Elaine R
Hultgren Scott J
Gordon Jeffrey I
References (61)
61 references, click to expand
  1. Complete genome sequence and comparative genomics of Shigella flexneri serotype 2a strain 2457T.
    Infect Immun. 2003 May;71(5):2775-86 PMID: 12704152
  2. Recombination and the population structures of bacterial pathogens.
    Annu Rev Microbiol. 2001;55:561-90 PMID: 11544367
  3. Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites.
    Genetics. 2003 Jul;164(3):1229-36 PMID: 12871927
  4. Sequence divergence, functional constraint, and selection in protein evolution.
    Annu Rev Genomics Hum Genet. 2003;4:213-35 PMID: 14527302
  5. Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis.
    Proc Natl Acad Sci U S A. 2004 Feb 3;101(5):1333-8 PMID: 14739341
  6. False-positive selection identified by ML-based methods: examples from the Sig1 gene of the diatom Thalassiosira weissflogii and the tax gene of a human T-cell lymphotropic virus.
    Mol Biol Evol. 2004 May;21(5):914-21 PMID: 15014169
  7. Of mice and men: phylogenetic footprinting aids the discovery of regulatory elements.
    J Biol. 2003;2(2):11 PMID: 12814519
  8. Divergence of conserved non-coding sequences: rate estimates and relative rate tests.
    Mol Biol Evol. 2004 Nov;21(11):2116-21 PMID: 15282332
  9. Transcriptome of uropathogenic Escherichia coli during urinary tract infection.
    Infect Immun. 2004 Nov;72(11):6373-81 PMID: 15501767
  10. Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites.
    Genetics. 2004 Oct;168(2):1041-51 PMID: 15514074
  11. Biosynthesis of enterochelin in Escherichia coli K-12: separation of the polypeptides coded for by the entD, E, F and G genes.
    Biochim Biophys Acta. 1979 Jan 4;582(1):145-53 PMID: 216414
  12. Iron and infection.
    Microbiol Rev. 1978 Mar;42(1):45-66 PMID: 379572
  13. Statistical tests for detecting gene conversion.
    Mol Biol Evol. 1989 Sep;6(5):526-38 PMID: 2677599
  14. OmpC is involved in invasion of epithelial cells by Shigella flexneri.
    Infect Immun. 1993 Sep;61(9):3625-35 PMID: 8359885
  15. Clonal divergence in Escherichia coli as a result of recombination, not mutation.
    Science. 1994 Nov 25;266(5189):1380-3 PMID: 7973728
  16. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  17. Distribution of enteric bacteria in Antarctic seawater surrounding a sewage outfall.
    Water Res. 1993 Apr;27(4):645-50 PMID: 11537610
  18. A program for calculating and displaying compatibility matrices as an aid in determining reticulate evolution in molecular sequences.
    Comput Appl Biosci. 1996 Aug;12(4):291-5 PMID: 8902355
  19. Common themes in microbial pathogenicity revisited.
    Microbiol Mol Biol Rev. 1997 Jun;61(2):136-69 PMID: 9184008
  20. Role of lipopolysaccharide and related cytokines in Helicobacter pylori infection.
    Recenti Prog Med. 1997 May;88(5):237-41 PMID: 9200967
  21. The complete genome sequence of Escherichia coli K-12.
    Science. 1997 Sep 5;277(5331):1453-62 PMID: 9278503
  22. PAML: a program package for phylogenetic analysis by maximum likelihood.
    Comput Appl Biosci. 1997 Oct;13(5):555-6 PMID: 9367129
  23. CedA is a novel Escherichia coli protein that activates the cell division inhibited by chromosomal DNA over-replication.
    Mol Microbiol. 1997 Nov;26(4):687-97 PMID: 9427399
  24. Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin.
    Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8922-6 PMID: 9671780
  25. Genomic analysis of a pathogenicity island in uropathogenic Escherichia coli CFT073: distribution of homologous sequences among isolates from patients with pyelonephritis, cystitis, and Catheter-associated bacteriuria and from fecal samples.
    Infect Immun. 1998 Sep;66(9):4411-7 PMID: 9712795
  26. Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli.
    Science. 1998 Nov 20;282(5393):1494-7 PMID: 9822381
  27. Cytokine responses during mucosal infections: role in disease pathogenesis and host defence.
    Curr Opin Microbiol. 1999 Feb;2(1):99-105 PMID: 10047563
  28. Virulence factor profiles and phylogenetic background of Escherichia coli isolates from veterans with bacteremia and uninfected control subjects.
    J Infect Dis. 2004 Dec 15;190(12):2121-8 PMID: 15551210
  29. EcoCyc: a comprehensive database resource for Escherichia coli.
    Nucleic Acids Res. 2005 Jan 1;33(Database issue):D334-7 PMID: 15608210
  30. Combined inactivation and expression strategy to study gene function under physiological conditions: application to identification of new Escherichia coli adhesins.
    J Bacteriol. 2005 Feb;187(3):1001-13 PMID: 15659678
  31. Optimization of virulence functions through glucosylation of Shigella LPS.
    Science. 2005 Feb 25;307(5713):1313-7 PMID: 15731456
  32. The relative contributions of recombination and mutation to the divergence of clones of Neisseria meningitidis.
    Mol Biol Evol. 1999 Nov;16(11):1496-502 PMID: 10555280
  33. RecBCD enzyme overproduction impairs DNA repair and homologous recombination in Escherichia coli.
    Res Microbiol. 2005 Apr;156(3):304-11 PMID: 15808933
  34. Mutator phenotype confers advantage in Escherichia coli chronic urinary tract infection pathogenesis.
    FEMS Immunol Med Microbiol. 2005 Jun 1;44(3):317-21 PMID: 15907455
  35. The Escherichia coli CpxA-CpxR envelope stress response system regulates expression of the porins ompF and ompC.
    J Bacteriol. 2005 Aug;187(16):5723-31 PMID: 16077119
  36. Evidence of positive Darwinian selection in putative meningococcal vaccine antigens.
    J Mol Evol. 2005 Jul;61(1):90-8 PMID: 16007491
  37. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome".
    Proc Natl Acad Sci U S A. 2005 Sep 27;102(39):13950-5 PMID: 16172379
  38. Molecular epidemiologic approaches to urinary tract infection gene discovery in uropathogenic Escherichia coli.
    Infect Immun. 2000 Apr;68(4):2009-15 PMID: 10722596
  39. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells.
    EMBO J. 2000 Jun 15;19(12):2803-12 PMID: 10856226
  40. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7.
    Nature. 2001 Jan 25;409(6819):529-33 PMID: 11206551
  41. Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12.
    DNA Res. 2001 Feb 28;8(1):11-22 PMID: 11258796
  42. A subtractive hybridisation analysis of genomic differences between the uropathogenic E. coli strain 536 and the E. coli K-12 strain MG1655.
    FEMS Microbiol Lett. 2001 May 15;199(1):61-6 PMID: 11356568
  43. In vivo requirement for RecJ, ExoVII, ExoI, and ExoX in methyl-directed mismatch repair.
    Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6765-70 PMID: 11381137
  44. A simulation study of the reliability of recombination detection methods.
    Mol Biol Evol. 2001 Oct;18(10):1929-39 PMID: 11557798
  45. Methods to detect selection in populations with applications to the human.
    Annu Rev Genomics Hum Genet. 2000;1:539-59 PMID: 11701640
  46. Reliabilities of parsimony-based and likelihood-based methods for detecting positive selection at single amino acid sites.
    Mol Biol Evol. 2001 Dec;18(12):2179-85 PMID: 11719567
  47. High frequency of mutator strains among human uropathogenic Escherichia coli isolates.
    J Bacteriol. 2002 Jan;184(2):605-9 PMID: 11751844
  48. Evaluation of methods for detecting recombination from DNA sequences: empirical data.
    Mol Biol Evol. 2002 May;19(5):708-17 PMID: 11961104
  49. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages.
    Mol Biol Evol. 2002 Jun;19(6):908-17 PMID: 12032247
  50. Accuracy and power of bayes prediction of amino acid sites under positive selection.
    Mol Biol Evol. 2002 Jun;19(6):950-8 PMID: 12032251
  51. Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157.
    Nucleic Acids Res. 2002 Oct 15;30(20):4432-41 PMID: 12384590
  52. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli.
    Proc Natl Acad Sci U S A. 2002 Dec 24;99(26):17020-4 PMID: 12471157
  53. Genome-tools: a flexible package for genome sequence analysis.
    Biotechniques. 2002 Dec;33(6):1334-41 PMID: 12503321
  54. Identification of a gene encoding heat-resistant agglutinin in Escherichia coli as a putative virulence factor in urinary tract infection.
    J Clin Microbiol. 2003 Jan;41(1):285-9 PMID: 12517862
  55. Regulation of Salmonella typhimurium lipopolysaccharide O antigen chain length is required for virulence; identification of FepE as a second Wzz.
    Mol Microbiol. 2003 Mar;47(5):1395-406 PMID: 12603743
  56. Topoisomerase III can serve as the cellular decatenase in Escherichia coli.
    J Biol Chem. 2003 Mar 7;278(10):8653-60 PMID: 12509418
  57. Establishment of a persistent Escherichia coli reservoir during the acute phase of a bladder infection.
    Infect Immun. 2001 Jul;69(7):4572-9 PMID: 11402001
  58. Involvement of N-acetylmuramyl-L-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli.
    Mol Microbiol. 2001 Jul;41(1):167-78 PMID: 11454209
  59. Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution.
    Mol Biol Evol. 2001 Aug;18(8):1585-92 PMID: 11470850
  60. Redundant exonuclease involvement in Escherichia coli methyl-directed mismatch repair.
    J Biol Chem. 2001 Aug 17;276(33):31053-8 PMID: 11418610
  61. Intracellular bacterial biofilm-like pods in urinary tract infections.
    Science. 2003 Jul 4;301(5629):105-7 PMID: 12843396
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
DOI
10.1073/pnas.0600938103
Published
2006-04-11
Epub
2006-00-03
Pages
5977-82
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1424661
Subset
IM
Grants
NIDDK NIH HHS · P50 DK064540 · United States
NIDDK NIH HHS · R01 DK051406 · United States
NHGRI NIH HHS · T32 HG000045 · United States
NIAMS NIH HHS · P50-AR049475 · United States
NHGRI NIH HHS · T32HG000045 · United States
NIDDK NIH HHS · DK51406 · United States
NIDDK NIH HHS · DK64540 · United States
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External Links
PubMed source DOI: 10.1073/pnas.0600938103 PMC Full Text View journal details
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