Identification of a modular pathogenicity island that is widespread among urease-producing uropathogens and shares features with a diverse group of mobile elements

Infection and Immunity

Volumn 77, Issue 11, 2009, Pages 4887-4894

  Flannery, Erika L ^a   Mody, Lona ^b,c   Mobley, Harry L T ^b  

^a UNIVERSITY OF MICHIGAN SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c VA ANN ARBOR HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL VIRULENCE; CATHETER INFECTION; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; CORYNEBACTERIUM XEROSIS; DNA SEQUENCE; GENE LOCUS; GENOMIC ISLAND; MORGANELLA MORGANII; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PATHOGENICITY ISLAND; PRIORITY JOURNAL; PROTEUS MIRABILIS; PROVIDENCIA STUARTII; URINARY TRACT INFECTION; YERSINIA;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; COMPARATIVE GENOMIC HYBRIDIZATION; DNA, BACTERIAL; ENTEROBACTERIACEAE INFECTIONS; GENE TRANSFER, HORIZONTAL; GENOMIC ISLANDS; HUMANS; INTERSPERSED REPETITIVE SEQUENCES; MOLECULAR SEQUENCE DATA; MORGANELLA MORGANII; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION; PROTEUS MIRABILIS; PROVIDENCIA; SEQUENCE HOMOLOGY, AMINO ACID; UREASE; URINARY TRACT INFECTIONS; VIRULENCE; VIRULENCE FACTORS;

EID: 70350461430     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00705-09     Document Type: Article

References (52)

1. Ahmed, N., U. Dobrindt, J. Hacker, and S. E. Hasnain. 2008. Genomic fluidity and pathogenic bacteria: applications in diagnostics, epidemiology, and intervention. Nat. Rev. Microbiol. 6:387-394.
2. Alamuri, P., K. A. Eaton, S. D. Himpsl, S. N. Smith, and H. L. Mobley. 2009. Vaccination with Proteus toxic agglutinin, a hemolysin-independent cytotoxin in vivo, protects against Proteus mirabilis urinary tract infection. Infect. Immun. 77:632-641.
3. Alamuri, P., and H. L. Mobley. 2008. A novel autotransporter of uropathogenic Proteus mirabilis is both a cytotoxin and an agglutinin. Mol. Microbiol. 68:997-1017.
4. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
5. Bach, S., A. de Almeida, and E. Carniel. 2000. The Yersinia high-pathogenicity island is present in different members of the family Enterobacteriaceae. FEMS Microbiol. Lett. 183:289-294. (Pubitemid 30079663)
6. Bell, K. S., M. Sebaihia, L. Pritchard, M. T. Holden, L. J. Hyman, M. C. Holeva, N. R. Thomson, S. D. Bentley, L. J. Churcher, K. Mungall, R. Atkin, N. Bason, K. Brooks, T. Chillingworth, K. Clark, J. Doggett, A. Fraser, Z. Hance, H. Hauser, K. Jagels, S. Moule, H. Norbertczak, D. Ormond, C. Price, M. A. Quail, M. Sanders, D. Walker, S. Whitehead, G. P. Salmond, P. R. Birch, J. Parkhill, and I. K. Toth. 2004. Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc. Natl. Acad. Sci. USA 101:11105-11110.
7. Buchrieser, C., R. Brosch, S. Bach, A. Guiyoule, and E. Carniel. 1998. The high-pathogenicity island of Yersinia pseudotuberculosis can be inserted into any of the three chromosomal asn tRNA genes. Mol. Microbiol. 30:965-978. (Pubitemid 28550121)
8. Bueno, S. M., C. A. Santiviago, A. A. Murillo, J. A. Fuentes, A. N. Trombert, P. I. Rodas, P. Youderian, and G. C. Mora. 2004. Precise excision of the large pathogenicity island, SPI7, in Salmonella enterica serovar Typhi. J. Bacteriol. 186:3202-3213.
9. Burall, L. S., J. M. Harro, X. Li, C. V. Lockatell, S. D. Himpsl, J. R. Hebel, D. E. Johnson, and H. L. Mobley. 2004. Proteus mirabilis genes that contribute to pathogenesis of urinary tract infection: identification of 25 signaturetagged mutants attenuated at least 100-fold. Infect. Immun. 72:2922-2938.
10. Burrus, V., G. Pavlovic, B. Decaris, and G. Guedon. 2002. Conjugative transposons: the tip of the iceberg. Mol. Microbiol. 46:601-610.
11. Burrus, V., and M. K. Waldor. 2004. Shaping bacterial genomes with integrative and conjugative elements. Res. Microbiol. 155:376-386.
12. Carniel, E., I. Guilvout, and M. Prentice. 1996. Characterization of a large chromosomal "high-pathogenicity island" in biotype 1B Yersinia enterocolitica. J. Bacteriol. 178:6743-6751.
13. Dobrindt, U., B. Hochhut, U. Hentschel, and J. Hacker. 2004. Genomic islands in pathogenic and environmental microorganisms. Nat. Rev. Microbiol. 2:414-424.
14. Duchaud, E., C. Rusniok, L. Frangeul, C. Buchrieser, A. Givaudan, S. Taourit, S. Bocs, C. Boursaux-Eude, M. Chandler, J. F. Charles, E. Dassa, R. Derose, S. Derzelle, G. Freyssinet, S. Gaudriault, C. Medigue, A. Lanois, K. Powell, P. Siguier, R. Vincent, V. Wingate, M. Zouine, P. Glaser, N. Boemare, A. Danchin, and F. Kunst. 2003. The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens. Nat. Biotechnol. 21:1307-1313.
15. Fukiya, S., H. Mizoguchi, T. Tobe, and H. Mori. 2004. Extensive genomic diversity in pathogenic Escherichia coli and Shigella strains revealed by comparative genomic hybridization microarray. J. Bacteriol. 186:3911-3921.
16. Hacker, J., and E. Carniel. 2001. Ecological fitness, genomic islands and bacterial pathogenicity: a Darwinian view of the evolution of microbes. EMBO Rep. 2:376-381.
17. Hacker, J., and J. B. Kaper. 2000. Pathogenicity islands and the evolution of microbes. Annu. Rev. Microbiol. 54:641-679.
18. Hassemna, J., J. Hnath, K. Ong, and E. Snesrud. 2006. Hybridization of labeled DNA and cDNA probes, p.8, 2nd ed., vol.M009. The Institute for Genomic Research, Rockville, MD.
19. Hassemna, J., J. Hnath, K. Ong, and E. Snesrud. 2006. Microbial genomic DNA aminoallyl labeling for microarrays, p.8, 2nd ed., vol.M009. The Institute for Genomic Research, Rockville, MD.
20. He, J., R. L. Baldini, E. Deziel, M. Saucier, Q. Zhang, N. T. Liberati, D. Lee, J. Urbach, H. M. Goodman, and L. G. Rahme. 2004. The broad host range pathogen Pseudomonas aeruginosa strain PA14 carries two pathogenicity islands harboring plant and animal virulence genes. Proc. Natl. Acad. Sci. USA 101:2530-2535.
21. Juhas, M., D. W. Crook, I. D. Dimopoulou, G. Lunter, R. M. Harding, D. J. Ferguson, and D. W. Hood. 2007. Novel type IV secretion system involved in propagation of genomic islands. J. Bacteriol. 189:761-771. (Pubitemid 46183850)
22. Juhas, M., D. W. Crook, and D. W. Hood. 2008. Type IV secretion systems: tools of bacterial horizontal gene transfer and virulence. Cell Microbiol. 10:2377-2386.
23. Juhas, M., P. M. Power, R. M. Harding, D. J. Ferguson, I. D. Dimopoulou, A. R. Elamin, Z. Mohd-Zain, D. W. Hood, R. Adegbola, A. Erwin, A. Smith, R. S. Munson, A. Harrison, L. Mansfield, S. Bentley, and D. W. Crook. 2007. Sequence and functional analyses of Haemophilus spp. genomic islands. Genome Biol. 8:R237.
24. Juhas, M., J. R. van der Meer, M. Gaillard, R. M. Harding, D. W. Hood, and D. W. Crook. 2009. Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol. Rev. 33:376-393.
25. Kim, C. C., E. A. Joyce, K. Chan, and S. Falkow. 2002. Improved analytical methods for microarray-based genome-composition analysis. Genome Biol. 3:RESEARCH0065.
26. Koonin, E. V., K. S. Makarova, and L. Aravind. 2001. Horizontal gene transfer in prokaryotes: quantification and classification. Annu. Rev. Microbiol. 55:709-742.
27. Lin, T. L., C. Z. Lee, P. F. Hsieh, S. F. Tsai, and J. T. Wang. 2008. Characterization of integrative and conjugative element ICEKp1-associated genomic heterogeneity in a Klebsiella pneumoniae strain isolated from a primary liver abscess. J. Bacteriol. 190:515-526.
28. Macleod, S. M., and D. J. Stickler. 2007. Species interactions in mixedcommunity crystalline biofilms on urinary catheters. J. Med. Microbiol. 56: 1549-1557.
29. Manos, J., and R. Belas. 2006. The genera Proteus, Providencia, and Morganella, p. 245-269. In M. Dworkin et al. (ed.), Prokaryotes: a handbook on the biology of bacteria. Springer, New York, NY.
30. Mathur, S., N. A. Sabbuba, M. T. Suller, D. J. Stickler, and R. C. Feneley. 2005. Genotyping of urinary and fecal Proteus mirabilis isolates from individuals with long-term urinary catheters. Eur. J. Clin. Microbiol. Infect. Dis. 24:643-644.
31. Minoia, M., M. Gaillard, F. Reinhard, M. Stojanov, V. Sentchilo, and J. R. van der Meer. 2008. Stochasticity and bistability in horizontal transfer control of a genomic island in Pseudomonas. Proc. Natl. Acad. Sci. USA 105: 20792-20797.
32. Mobley, H. L., and J. W. Warren. 1987. Urease-positive bacteriuria and obstruction of long-term urinary catheters. J. Clin. Microbiol. 25:2216-2217.
33. Mody, L., S. Maheshwari, A. Galecki, C. A. Kauffman, and S. F. Bradley. 2007. Indwelling device use and antibiotic resistance in nursing homes: identifying a high-risk group. J. Am. Geriatr. Soc. 55:1921-1926.
34. Mohd-Zain, Z., S. L. Turner, A. M. Cerdeno-Tarraga, A. K. Lilley, T. J. Inzana, A. J. Duncan, R. M. Harding, D. W. Hood, T. E. Peto, and D. W. Crook. 2004. Transferable antibiotic resistance elements in Haemophilus influenzae share a common evolutionary origin with a diverse family of syntenic genomic islands. J. Bacteriol. 186:8114-8122.
35. Murray, M. G., and W. F. Thompson. 1980. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 8:4321-4325.
36. Nair, S., S. Alokam, S. Kothapalli, S. Porwollik, E. Proctor, C. Choy, M. McClelland, S. L. Liu, and K. E. Sanderson. 2004. Salmonella enterica serovar Typhi strains from which SPI7, a 134-kilobase island with genes for Vi exopolysaccharide and other functions, has been deleted. J. Bacteriol. 186:3214-3223.
37. Nielubowicz, G. R., S. N. Smith, and H. L. Mobley. 2008. Outer membrane antigens of the uropathogen Proteus mirabilis recognized by the humoral response during experimental murine urinary tract infection. Infect. Immun. 76:4222-4231.
38. Pallen, M. J., and B. W. Wren. 2007. Bacterial pathogenomics. Nature 449:835-842.
39. Parkhill, J., G. Dougan, K. D. James, N. R. Thomson, D. Pickard, J. Wain, C. Churcher, K. L. Mungall, S. D. Bentley, M. T. Holden, M. Sebaihia, S. Baker, D. Basham, K. Brooks, T. Chillingworth, P. Connerton, A. Cronin, P. Davis, R. M. Davies, L. Dowd, N. White, J. Farrar, T. Feltwell, N. Hamlin, A. Haque, T. T. Hien, S. Holroyd, K. Jagels, A. Krogh, T. S. Larsen, S. Leather, S. Moule, P. O'Gaora, C. Parry, M. Quail, K. Rutherford, M. Simmonds, J. Skelton, K. Stevens, S. Whitehead, and B. G. Barrell. 2001. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413:848-852.
40. Pickard, D., J. Wain, S. Baker, A. Line, S. Chohan, M. Fookes, A. Barron, P. O. Gaora, J. A. Chabalgoity, N. Thanky, C. Scholes, N. Thomson, M. Quail, J. Parkhill, and G. Dougan. 2003. Composition, acquisition, and distribution of the Vi exopolysaccharide-encoding Salmonella enterica pathogenicity island SPI-7. J. Bacteriol. 185:5055-5065.
41. Qiu, X., A. U. Gurkar, and S. Lory. 2006. Interstrain transfer of the large pathogenicity island (PAPI-1) of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 103:19830-19835.
42. Rutherford, K., J. Parkhill, J. Crook, T. Horsnell, P. Rice, M. A. Rajandream, and B. Barrell. 2000. Artemis: sequence visualization and annotation. Bioinformatics 16:944-945.
43. Saeed, A. I., V. Sharov, J. White, J. Li, W. Liang, N. Bhagabati, J. Braisted, M. Klapa, T. Currier, M. Thiagarajan, A. Sturn, M. Snuffin, A. Rezantsev, D. Popov, A. Ryltsov, E. Kostukovich, I. Borisovsky, Z. Liu, A. Vinsavich, V. Trush, and J. Quackenbush. 2003. TM4: a free, open-source system for microarray data management and analysis. BioTechniques 34:374-378.
44. Saldanha, A. J. 2004. Java TreeView: extensible visualization of microarray data. Bioinformatics 20:3246-3248.
45. Schubert, S., S. Cuenca, D. Fischer, and J. Heesemann. 2000. High-pathogenicity island of Yersinia pestis in Enterobacteriaceae isolated from blood cultures and urine samples: prevalence and functional expression. J. Infect. Dis. 182:1268-1271.
46. Schubert, S., S. Dufke, J. Sorsa, and J. Heesemann. 2004. A novel integrative and conjugative element (ICE) of Escherichia coli: the putative progenitor of the Yersinia high-pathogenicity island. Mol. Microbiol. 51:837-848.
47. Schubert, S., A. Rakin, H. Karch, E. Carniel, and J. Heesemann. 1998. Prevalence of the "high-pathogenicity island" of Yersinia species among Escherichia coli strains that are pathogenic to humans. Infect. Immun. 66: 480-485.
48. Seth-Smith, H., and N. J. Croucher. 2009. Genome watch: breaking the ICE. Nat. Rev. Microbiol. 7:328-329.
49. Tambyah, P. A., and D. G. Maki. 2000. Catheter-associated urinary tract infection is rarely symptomatic: a prospective study of 1,497 catheterized patients. Arch. Intern. Med. 160:678-682.
50. Thomson, N. R., S. Howard, B. W. Wren, M. T. Holden, L. Crossman, G. L. Challis, C. Churcher, K. Mungall, K. Brooks, T. Chillingworth, T. Feltwell, Z. Abdellah, H. Hauser, K. Jagels, M. Maddison, S. Moule, M. Sanders, S. Whitehead, M. A. Quail, G. Dougan, J. Parkhill, and M. B. Prentice. 2006. The complete genome sequence and comparative genome analysis of the high pathogenicity Yersinia enterocolitica strain 8081. PLoS Genet. 2:e206.
51. Warren, J. W., J. H. Tenney, J. M. Hoopes, H. L. Muncie, and W. C. Anthony. 1982. A prospective microbiologic study of bacteriuria in patients with chronic indwelling urethral catheters. J. Infect. Dis. 146:719-723.
52. Wray, S. K., S. I. Hull, R. G. Cook, J. Barrish, and R. A. Hull. 1986. Identification and characterization of a uroepithelial cell adhesin from a uropathogenic isolate of Proteus mirabilis. Infect. Immun. 54:43-49.