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A virulent parent with probiotic progeny: comparative genomics of Escherichia coli strains CFT073, Nissle 1917 and ABU 83972

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Abstract

Escherichia coli is a highly versatile species encompassing a diverse spectrum of strains, i.e. from highly virulent isolates causing serious infectious diseases to commensals and probiotic strains. Although much is known about bacterial pathogenicity in E. coli, the understanding of which genetic determinants differentiates a virulent from an avirulent strain still remains limited. In this study we designed a new comparative genomic hybridization microarray based on 31 sequenced E. coli strains and used it to compare two E. coli strains used as prophylactic agents (i.e. Nissle 1917 and 83972) with the highly virulent uropathogen CFT073. Only relatively minor genetic variations were found between the isolates, suggesting that the three strains may have originated from the same virulent ancestral parent. Interestingly, Nissle 1917 (a gut commensal strain) was more similar to CFT073 with respect to genotype and phenotype than 83972 (an asymptomatic bacteriuria strain). The study indicates that genetic variations (e.g. mutations) and expression differences, rather than genomic content per se, contribute to the divergence in disease-causing ability between these strains. This has implications for the use of virulence factors in epidemiological research, and emphasizes the need for more comparative genomic studies of closely related strains to compare their virulence potential.

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References

  • Alteri CJ, Mobley HL (2007) Quantitative profile of the uropathogenic Escherichia coli outer membrane proteome during growth in human urine. Infect Immun 75(6):2679–2688

    CAS  PubMed  Google Scholar 

  • Andersson P, Engberg I, Lidin-Janson G, Lincoln K, Hull R, Hull S, Svanborg C (1991) Persistence of Escherichia coli bacteriuria is not determined by bacterial adherence. Infect Immun 59:2915–2921

    CAS  PubMed  Google Scholar 

  • Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL (2008) GenBank. Nucleic Acids Res 36:D25–D30

    Article  CAS  PubMed  Google Scholar 

  • Bhargava S, Johnson BB, Hwang J, Harris TA, George AS, Muir A, Dorff J, Okeke IN (2009) Heat-resistant agglutinin 1 is an accessory enteroaggregative Escherichia coli colonization factor. J Bacteriol 191:4934–4942

    Article  CAS  PubMed  Google Scholar 

  • 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 (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

    Article  CAS  PubMed  Google Scholar 

  • Chouikha I, Germon P, Bree A, Gilot P, Moulin-Schouleur M, Schouler C (2006) A selC-associated genomic island of the extraintestinal avian pathogenic Escherichia coli strain BEN2908 is involved in carbohydrate uptake and virulence. J Bacteriol 188:977–987

    Article  CAS  PubMed  Google Scholar 

  • Cirl C, Wieser A, Yadav M, Duerr S, Schubert S, Fischer H, Stappert D, Wantia N, Rodriguez N, Wagner H, Svanborg C, Miethke T (2008) Subversion of Toll-like receptor signaling by a unique family of bacterial Toll/interleukin-1 receptor domain-containing proteins. Nat Med 14:399–406

    Article  CAS  PubMed  Google Scholar 

  • Connell H, Agace W, Klemm P, Schembri M, Marild S, Svanborg C (1996) Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc Natl Acad Sci USA 93:9827–9832

    Article  CAS  PubMed  Google Scholar 

  • Croxen MA, Finlay BB (2010) Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 8:26–38

    Article  CAS  PubMed  Google Scholar 

  • Danese PN, Pratt LA, Dove SL, Kolter R (2000) The outer membrane protein, antigen 43, mediates cell-to-cell interactions within Escherichia coli biofilms. Mol Microbiol 37:424–432

    Article  CAS  PubMed  Google Scholar 

  • Dobrindt U, Hentschel U, Kaper JB, Hacker J (2002) Genome plasticity in pathogenic and nonpathogenic enterobacteria. Curr Top Microbiol Immunol 264:157–175

    CAS  PubMed  Google Scholar 

  • Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80

    Article  PubMed  Google Scholar 

  • Gottesman S, Stout V (1991) Regulation of capsular polysaccharide synthesis in Escherichia coli K12. Mol Microbiol 5:1599–1606

    Article  CAS  PubMed  Google Scholar 

  • Grozdanov L, Zahringer U, Blum-Oehler G, Brade L, Henne A, Knirel YA, Schombel U, Schulze J, Sonnenborn U, Gottschalk G, Hacker J, Rietschel ET, Dobrindt U (2002) A single nucleotide exchange in the wzy gene is responsible for the semirough O6 lipopolysaccharide phenotype and serum sensitivity of Escherichia coli strain Nissle 1917. J Bacteriol 184:5912–5925

    Article  CAS  PubMed  Google Scholar 

  • Grozdanov L, Raasch C, Schulze J, Sonnenborn U, Gottschalk G, Hacker J, Dobrindt U (2004) Analysis of the genome structure of the nonpathogenic probiotic Escherichia coli strain Nissle 1917. J Bacteriol 186:5432–5441

    Article  CAS  PubMed  Google Scholar 

  • Hacker J, Carniel E (2001) Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes. EMBO Rep 2:376–381

    CAS  PubMed  Google Scholar 

  • Hafez M, Hayes K, Goldrick M, Warhurst G, Grencis R, Roberts IS (2009) The K5 capsule of Escherichia coli strain Nissle 1917 is important in mediating interactions with intestinal epithelial cells and chemokine induction. Infect Immun 77:2995–3003

    Article  CAS  PubMed  Google Scholar 

  • Hagan EC, Mobley HL (2007) Uropathogenic Escherichia coli outer membrane antigens expressed during urinary tract infection. Infect Immun 75:3941–3949

    Article  CAS  PubMed  Google Scholar 

  • Hancock V, Klemm P (2007) Global gene expression profiling of asymptomatic bacteriuria Escherichia coli during biofilm growth in human urine. Infect Immun 75:966–976

    Article  CAS  PubMed  Google Scholar 

  • Hancock V, Ferrières L, Klemm P (2007) Biofilm formation by asymptomatic and virulent urinary tract infectious Escherichia coli strains. FEMS Microbiol Lett 267:30–37

    Article  CAS  PubMed  Google Scholar 

  • Hancock V, Seshasayee AS, Ussery DW, Luscombe NM, Klemm P (2008) Transcriptomics and adaptive genomics of the asymptomatic bacteriuria Escherichia coli strain 83972. Mol Genet Genomics 279:523–534

    Article  CAS  PubMed  Google Scholar 

  • Hancock V, Nielsen EM, Krag L, Engberg J, Klemm P (2009) Comparative analysis of antibiotic resistance and phylogenetic group patterns in human and porcine urinary tract infectious Escherichia coli. APMIS 117:786–790

    Article  CAS  PubMed  Google Scholar 

  • Hannan TJ, Mysorekar IU, Chen SL, Walker JN, Jones JM, Pinkner JS, Hultgren SJ, Seed PC (2008) LeuX tRNA-dependent and -independent mechanisms of Escherichia coli pathogenesis in acute cystitis. Mol Microbiol 67:116–128

    Google Scholar 

  • Hentschel U, Hacker J (2001) Pathogenicity islands: the tip of the iceberg. Microbes Infect 3:545–548

    Article  CAS  PubMed  Google Scholar 

  • Hobohm U, Scharf M, Schneider R, Sander C (1992) Selection of representative protein data sets. Protein Sci 1:409–417

    Article  CAS  PubMed  Google Scholar 

  • Hull RA, Rudy DC, Donovan WH, Wieser IE, Stewart C, Darouiche RO (1999) Virulence properties of Escherichia coli 83972, a prototype strain associated with asymptomatic bacteriuria. Infect Immun 67:429–432

    CAS  PubMed  Google Scholar 

  • Hull R, Rudy D, Donovan W, Svanborg C, Wieser I, Stewart C, Darouiche R (2000) Urinary tract infection prophylaxis using Escherichia coli 83972 in spinal cord injured patients. J Urol 163:872–877

    Article  CAS  PubMed  Google Scholar 

  • Johanson IM, Plos K, Marklund BI, Svanborg C (1993) Pap, papG and prsG DNA sequences in Escherichia coli from the fecal flora and the urinary tract. Microb Pathog 15:121–129

    Article  CAS  PubMed  Google Scholar 

  • Kaper JB, Nataro JP, Mobley HL (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2:123–140

    Article  CAS  PubMed  Google Scholar 

  • Klemm P, Roos V, Ulett GC, Svanborg C, Schembri MA (2006) Molecular characterization of the Escherichia coli asymptomatic bacteriuria strain 83972: the taming of a pathogen. Infect Immun 74:781–785

    Article  CAS  PubMed  Google Scholar 

  • Klemm P, Hancock V, Schembri MA (2007) Mellowing out: adaptation to commensalism by Escherichia coli asymptomatic bacteriuria strain 83972. Infect Immun 75:3688–3695

    Article  CAS  PubMed  Google Scholar 

  • Kruis W, Schutz E, Fric P, Fixa B, Judmaier G, Stolte M (1997) Double-blind comparison of an oral Escherichia coli preparation and mesalazine in maintaining remission of ulcerative colitis. Aliment Pharmacol Ther 11:853–858

    Article  CAS  PubMed  Google Scholar 

  • Lane MC, Mobley HL (2007) Role of P-fimbrial-mediated adherence in pyelonephritis and persistence of uropathogenic Escherichia coli (UPEC) in the mammalian kidney. Kidney Int 72:19–25

    Article  CAS  PubMed  Google Scholar 

  • Larsen TS, Krogh A (2003) EasyGene—a prokaryotic gene finder that ranks ORFs by statistical significance. BMC Bioinformatics 4:21

    Article  PubMed  Google Scholar 

  • Lindberg U, Hanson LA, Jodal U, Lidin-Janson G, Lincoln K, Olling S (1975) Asymptomatic bacteriuria in schoolgirls. II. Differences in Escherichia coli causing asymptomatic bacteriuria. II. Differences in Escherichia coli causing asymptomatic bacteriuria. Acta Paediatr Scand 64:432–436

    Article  CAS  PubMed  Google Scholar 

  • Lloyd AL, Rasko DA, Mobley HL (2007) Defining genomic islands and uropathogen-specific genes in uropathogenic Escherichia coli. J Bacteriol 189:3532–3546

    Article  CAS  PubMed  Google Scholar 

  • Lloyd AL, Henderson TA, Vigil PD, Mobley HL (2009) Genomic islands of uropathogenic Escherichia coli contribute to virulence. J Bacteriol 191:3469–3481

    Article  CAS  PubMed  Google Scholar 

  • Malchow HA (1997) Crohn’s disease and Escherichia coli. A new approach in therapy to maintain remission of colonic Crohn’s disease? J Clin Gastroenterol 25:653–658

    Article  CAS  PubMed  Google Scholar 

  • Middendorf B, Hochhut B, Leipold K, Dobrindt U, Blum-Oehler G, Hacker J (2004) Instability of pathogenicity islands in uropathogenic Escherichia coli 536. J Bacteriol 186:3086–3096

    Article  CAS  PubMed  Google Scholar 

  • Mobley HL, Green DM, Trifillis AL, Johnson DE, Chippendale GR, Lockatell CV, Jones BD, Warren JW (1990) Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. Infect Immun 58:1281–1289

    CAS  PubMed  Google Scholar 

  • Monteiro C, Saxena I, Wang X, Kader A, Bokranz W, Simm R, Nobles D, Chromek M, Brauner A, Brown RM Jr, Romling U (2009) Characterization of cellulose production in Escherichia coli Nissle 1917 and its biological consequences. Environ Microbiol 11:1105–1116

    Article  CAS  PubMed  Google Scholar 

  • Nielsen P, Krogh A (2005) Large-scale prokaryotic gene prediction and comparison to genome annotation. Bioinformatics 21:4322–4329

    Article  CAS  PubMed  Google Scholar 

  • Nissle A (1918) Die antagonistische Behandlungen chronischer Darmstörungen mir Kolibakterien. Med Klein 2:29–30

    Google Scholar 

  • Nissle A (1925) Weiteres über Grundlagen und Praxis der Mutaflorbehandlung. DMW 4:1809–1813

    Google Scholar 

  • Prigent-Combaret C, Prensier G, Le Thi TT, Vidal O, Lejeune P, Dorel C (2000) Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environ Microbiol 2:450–464

    Article  CAS  PubMed  Google Scholar 

  • Roos V, Klemm P (2006) Global gene expression profiling of the asymptomatic bacteriuria Escherichia coli strain 83972 in the human urinary tract. Infect Immun 74:3565–3575

    Article  CAS  PubMed  Google Scholar 

  • Roos V, Ulett GC, Schembri MA, Klemm P (2006) The asymptomatic bacteriuria Escherichia coli strain 83972 out-competes UPEC strains in human urine. Infect Immun 74:615–624

    Article  CAS  PubMed  Google Scholar 

  • Russo TA, Carlino UB, Johnson JR (2001) Identification of a new iron-regulated virulence gene, ireA, in an extraintestinal pathogenic isolate of Escherichia coli. Infect Immun 69:6209–6216

    Article  CAS  PubMed  Google Scholar 

  • Schultz M (2008) Clinical use of E. coli Nissle 1917 in inflammatory bowel disease. Inflamm Bowel Dis 14:1012–1018

    Article  PubMed  Google Scholar 

  • Snyder JA, Haugen BJ, Buckles EL, Lockatell CV, Johnson DE, Donnenberg MS, Welch RA, Mobley HL (2004) Transcriptome of uropathogenic Escherichia coli during urinary tract infection. Infect Immun 72:6373–6381

    Article  CAS  PubMed  Google Scholar 

  • Sonnenborn U, Schulze J (2009) The non-pathogenic Escherichia coli strain Nissle 1917—features of a versatile probiotic. Microb Ecol Health Dis 21:122–158

    Article  CAS  Google Scholar 

  • Stamm WE (1991) Catheter-associated urinary tract infections: epidemiology, pathogenesis, and prevention. Am J Med 91:65S–71S

    Article  CAS  PubMed  Google Scholar 

  • Stapleton A, Moseley S, Stamm WE (1991) Urovirulence determinants in Escherichia coli isolates causing first-episode and recurrent cystitis in women. J Infect Dis 163:773–779

    CAS  PubMed  Google Scholar 

  • Stout V, Torres-Cabassa A, Maurizi MR, Gutnick D, Gottesman S (1991) RcsA, an unstable positive regulator of capsular polysaccharide synthesis. J Bacteriol 173:1738–1747

    CAS  PubMed  Google Scholar 

  • Sun J, Gunzer F, Westendorf AM, Buer J, Scharfe M, Jarek M, Gossling F, Blocker H, Zeng AP (2005) Genomic peculiarity of coding sequences and metabolic potential of probiotic Escherichia coli strain Nissle 1917 inferred from raw genome data. J Biotechnol 117:147–161

    Article  CAS  PubMed  Google Scholar 

  • Sunden F, Hakansson L, Ljunggren E, Wullt B (2006) Bacterial interference—is deliberate colonization with Escherichia coli 83972 an alternative treatment for patients with recurrent urinary tract infection? Int J Antimicrob Agents 28(Suppl 1):S26–S29

    Article  CAS  PubMed  Google Scholar 

  • Tischler AD, Camilli A (2004) Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 53:857–869

    Article  CAS  PubMed  Google Scholar 

  • Tischler AD, Camilli A (2005) Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect Immun 73:5873–5882

    Article  CAS  PubMed  Google Scholar 

  • Tseng CC, Huang JJ, Wang MC, Wu AB, Ko WC, Chen WC, Wu JJ (2007) PapG II adhesin in the establishment and persistence of Escherichia coli infection in mouse kidneys. Kidney Int 71:764–770

    Article  CAS  PubMed  Google Scholar 

  • Vejborg RM, Bernbom N, Gram L, Klemm P (2008) Anti-adhesive properties of fish tropomyosins. J Appl Microbiol 105:141–150

    Article  CAS  PubMed  Google Scholar 

  • Vianney A, Jubelin G, Renault S, Dorel C, Lejeune P, Lazzaroni JC (2005) Escherichia coli tol and rcs genes participate in the complex network affecting curli synthesis. Microbiology 151:2487–2497

    Article  CAS  PubMed  Google Scholar 

  • von Bargen K, Polidori M, Becken U, Huth G, Prescott JF, Haas A (2009) Rhodococcus equi virulence-associated protein A is required for diversion of phagosome biogenesis but not for cytotoxicity. Infect Immun 77:5676–5681

    Article  CAS  Google Scholar 

  • Welch RA, Burland V, Plunkett G 3rd, Redford P, Roesch P, Rasko D, Buckles EL, Liou SR, Boutin A, Hackett J, Stroud D, Mayhew GF, Rose DJ, Zhou S, Schwartz DC, Perna NT, Mobley HL, Donnenberg MS, Blattner FR (2002) Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci USA 99:17020–17024

    Article  CAS  PubMed  Google Scholar 

  • Wernersson R, Nielsen HB (2005) OligoWiz 2.0—integrating sequence feature annotation into the design of microarray probes. Nucleic Acids Res 33:W611–W615

    Article  CAS  PubMed  Google Scholar 

  • Wernersson R, Juncker AS, Nielsen HB (2007) Probe selection for DNA microarrays using OligoWiz. Nat Protoc 2:2677–2691

    Article  CAS  PubMed  Google Scholar 

  • Zdziarski J, Svanborg C, Wullt B, Hacker J, Dobrindt U (2008) Molecular basis of commensalism in the urinary tract: low virulence or virulence attenuation? Infect Immun 76:695–703

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants from Lundbeckfonden (grant no. R17-A1603) and the Danish Medical Research Council (271-06-0555). We also wish to thank the Danish Center for Scientific Computing (DCSC) and the Danish Natural Science Research Council (FNU grant 26-06-0349). MAS is supported by a grant from the National Health and Medical Research Council of Australia (569676).

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Authors and Affiliations

  1. DTU Food, Technical University of Denmark, Building 301, 2800, Lyngby, Denmark

    Rebecca Munk Vejborg, Carsten Friis, Viktoria Hancock & Per Klemm

  2. School of Chemistry and Molecular Biosciences, University of Queensland, Brisbane, Australia

    Mark A. Schembri

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  1. Rebecca Munk Vejborg
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  2. Carsten Friis
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  3. Viktoria Hancock
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Correspondence to Per Klemm.

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Communicated by D. Andersson.

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Vejborg, R.M., Friis, C., Hancock, V. et al. A virulent parent with probiotic progeny: comparative genomics of Escherichia coli strains CFT073, Nissle 1917 and ABU 83972. Mol Genet Genomics 283, 469–484 (2010). https://doi.org/10.1007/s00438-010-0532-9

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