Loss of Virulence Genes in Escherichia coli Populations during Manure Storage on a Commercial Swine Farm

Applied and Environmental Microbiology

Volumn 74, Issue 13, 2008, Pages 3935-3942

  Duriez, Patrick ^a   Zhang, Yun ^a   Lu, Zexun ^a   Scott, Andrew ^a   Topp, Edward ^a  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AGRICULTURAL WASTES; AGRICULTURE; ESCHERICHIA COLI; FERTILIZERS; HEALTH RISKS; MANURES; STORAGE (MATERIALS); TANKS (CONTAINERS);

COMMERCIAL FARMS; DIFFUSION CHAMBER; ENTERIC PATHOGENS; LAND APPLICATIONS; LIVESTOCK PRODUCTION; LOWER FREQUENCIES; NATURAL ENVIRONMENTS; POPULATION STRUCTURES;

GENES;

AGRICULTURAL RUNOFF; COMMERCIAL ACTIVITY; EXPERIMENTAL STUDY; FECAL COLIFORM; GENOTYPE; HEALTH RISK; INOCULATION; MANURE; PATHOGEN; PIG; POLYMERASE CHAIN REACTION; POPULATION STRUCTURE; PUBLIC HEALTH; SURVIVAL; VIRULENCE;

AGRICULTURAL WASTE; AIDA I GENE; ARTICLE; ASTA GENE; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; ESCHERICHIA COLI; ESTB GENE; FEDA GENE; GENETIC STABILITY; GENOTYPE; HEALTH HAZARD; MANURE; NONHUMAN; PAA GENE; PIG FARMING; POLYMERASE CHAIN REACTION; POPULATION STRUCTURE; SEPA GENE; STORAGE; STX 2E GENE;

ASTA; ESCHERICHIA COLI; PAA; SUIDAE;

EID: 46949100112     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02710-07     Document Type: Article

References (53)

1. Alsam, S., S. R. Jeong, J. Sissons, R. Dudley, K. S. Kim, and N. A. Khan. 2006. Escherichia coli interactions with Acanthamoeba: a symbiosis with environmental and clinical implications. J. Med. Microbiol. 55:689-694.
2. Ball Coelho, B. R., R. C. Roy, E. Topp, and D. R. Lapen. 2007. Tile water quality following liquid swine manure application into standing corn. J. Environ. Qual. 36:580-587.
3. Beaulieu, M. S. 2004. Manure management in Canada. In R. Koroluk (ed.), Farm environmental management survey, vol. 1. Statistics Canada, Ottawa, Canada.
4. Benjelloun-Touimi, Z., P. J. Sansonetti, and C. Parsot. 1995. SepA, the major extracellular protein of Shigella flexneri: autonomous secretion and involvement in tissue invasion. Mol. Microbiol. 17:123-135.
5. Benz, I., and M. A. Schmidt. 1989. Cloning and expression of an adhesin (AIDA-I) involved in diffuse adherence of enteropathogenic Escherichia coli. Infect. Immun. 57:1506-1511.
6. Boerlin, P., R. M. Travis, C. L. Gyles, R. Reid-Smith, N. Janecko, L. Heather, V. Nicholson, S. A. McEwen, R. M. Friendship, and M. Archambault. 2005. Antimicrobial resistance and virulence genes of Escherichia coli isolates from swine in Ontario. Appl. Environ. Microbiol. 71:6753-6761.
7. Bonacorsi, S., V. Houdouin, P. Mariani-Kurkdjian, F. Mahjoub-Messai, and E. Bingen. 2006. Comparative prevalence of virulence factors in Escherichia coli causing urinary tract infection in male infants with and without bacteremia. J. Clin. Microbiol. 44:1156-1158.
8. Bourque, L., and R. Koroluk. 2003. Manure storage in Canada. In R. Vani (ed.), Farm environmental management survey, vol. 1. Statistics Canada, Ottawa, Canada.
9. Brandl, M. T. 2006. Fitness of human enteric pathogens on plants and implications for food safety. Ann. Rev. Phytopathol. 44:367-392.
10. Collins, J. D., and P. G. Wall. 2004. Food safety and animal production systems: controlling zoonoses at farm level. Rev. Sci. Tech. 23:685-700.
11. Côté, C., A. Villeneuve, L. Lessard, and S. Quessy. 2006. Fate of pathogenic and nonpathogenic microorganisms during storage of liquid hog manure in Quebec: biosccurity of livestock effluents. Livestock Sci. 102:204-210.
12. Diarrassouba, F., M. S. Diarra, S. Bach, P. Delaquis, J. Pritchard, E. Topp, and B. J. Skura. 2007. Antibiotic resistance and virulence genes in commensal Escherichia coli and Salmonella isolates from commercial broiler chicken farms. J. Food Prot. 70:1316-1327.
13. Dobrindt, U., F. Agerer, K. Michaelis, A. Janka, C. Buchrieser, M. Samuelson, C. Svanborg, G. Gottschalk, H. Karch, and J. Hacker. 2003. Analysis of genome plasticity in pathogenic and commensal Escherichia coli isolates by use of DNA arrays. J. Bacteriol. 185:1831-1840.
14. Dobrindt, U., B. Hochhut, U. Hentschel, and J. Hacker. 2004. Genomic islands in pathogenic and environmental microorganisms. Nat. Rev. Microbiol. 2:414-424.
15. Duriez, P., O. Clermont, S. Bonacorsi, E. Bingen, A. Chaventré, J. Elion, B. Picard, and E. Denamur. 2001. Commensal Escherichia coli isolates are phylogenetically distributed among geographically distinct human populations. Microbiology 147:1671-1676.
16. Duriez, P., and E. Topp. 2007. Escherichia coli on a commercial swine farm: temporal dynamics, and impact of manure storage on patterns of antibiotic resistance and population structure. Appl. Environ. Microbiol. 73:5486-5493.
17. Edberg, S. C., E. W. Rice, R. J. Karlin, and M. J. Allen. 2000. Escherichia coli: the best biological drinking water indicator for public health protection. J. Appl. Microbiol. 88:106S-116S.
18. Elena, S. F., and R. E. Lenski. 2003. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat. Rev. Genet. 4:457-469.
19. Escobar-Páramo, P., O. Clermont, A.-B. Blanc-Potard, H. Bui, C. Le Bouguénec, and E. Denamur. 2004. A specific genetic background is required for acquisition and expression of virulence factors in Escherichia coli. Mol. Biol. Evol. 21:1085-1094.
20. Fewtrell, L., and J. Bartram. 2001. Water quality - guidelines, standards and health: assessment of risk and risk management for water-related infectious disease. World Health Organization, London, United Kingdom.
21. Franklin, A., and R. Möllby. 1983. Concurrent transfer and recombination between plasmids encoding for heat-stable enterotoxin and drug resistance in porcine enterotoxigenic Escherichia coli. Med. Microbiol. Immunol. 172:137-147.
22. Fux, C. A., M. Shirtliff, P. Stoodley, and J. W. Costerton. 2005. Can laboratory reference strains mirror "real-world" pathogenesis? Trends Microbiol. 13:58-63.
23. Gyles, C. L. 1994. Escherichia coli enterotoxins, p. 337-364. In C. L. Gyles (ed.), Escherichia coli in domestic animals and humans. CAB International, Wallingford, United Kingdom.
24. Gyles, C. L. 1994. Escherichia coli verotoxins and other cytotoxins, p. 365-398. In C. L. Gyles (ed.), Escherichia coli in domestic animals and humans. CAB International, Wallingford, United Kingdom.
25. Haas, C. N., J. B. Rose, and C. P. Gerba. 1999. Quantitative microbial risk assessment. John Wiley and Sons, Inc., New York, NY.
26. Hacker, J., and J. B. Kaper. 2000. Pathogenicity islands and the evolution of microbes. Ann. Rev. Microbiol. 54:641-679.
27. Hamelin, K., G. Bruant, A. El-Shaarawi, S. Hill, T. A. Edge, S. Bekal, J. M. Fairbrother, J. Harel, C. Maynard, L. Masson, and R. Brousseau. 2006. A virulence and antimicrobial resistance DNA microarray detects a high frequency of virulence genes in Escherichia coli isolates from Great Lakes recreational waters. Appl. Environ. Microbiol. 72:4200-4206.
28. Harnett, N. M., and C. L. Gyles. 1985. Enterotoxin plasmids in bovine and porcine enterotoxigenic Escherichia coli of 0 groups 9, 20, 64 and 101. Can. J. Comp. Med. 49:79-87.
29. Hutchison, M. L., L. D. Walters, A. Moore, and S. M. Avery. 2005. Declines of zoonotic agents in liquid livestock wastes stored in batches on-farm. J. Appl. Microbiol. 99:58-65.
30. Kaper, J. B., J. P. Nataro, and H. L. T. Mobley. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2:123-140.
31. Karch, H., S. Schubert, D. Zhang, W. Zhang, H. Schmidt, T. Ölschläger, and J. Hacker. 1999. A genomic island, termed high-pathogenicity island, is present in certain non-O157 Shiga toxin-producing Escherichia coli clonal lineages. Infect. Immun. 67:5994-6001.
32. Leclerc, S., P. Boerlin, C. Gyles, J. D. Dubreuil, M. Mourez, J. M. Fairbrother, and J. Harel. 2007. paa, originally identified in attaching and effacing Escherichia coli, is also associated with enterotoxigenic E. coli. Res. Microbiol. 158:97-104.
33. Lu, Z., D. Lapen, A. Scott, A. Dang, and E. Topp. 2005. Identifying host sources of fecal pollution: diversity of Escherichia coli in confined dairy and swine production systems. Appl. Environ. Microbiol. 71:5992-5998.
34. Mainil, J. G., G. Daube, E. Jacquemin, P. Pohl, and A. Kaeckenbeeck. 1998. Virulence plasmids of enterotoxigenic Escherichia coli isolates from piglets. Vet. Microbiol. 62:291-301.
35. Mainil, J. G., E. Jacquemin, P. Pohl, A. Kaeckenbeeck, and I. Benz. 2002. DNA sequences coding for the F18 fimbriae and AIDA adhesin are localised on the same plasmid in Escherichia coli isolates from piglets. Vet. Microbiol. 86:303-311.
36. Matz, C., and S. Kjelleberg. 2005. Off the hook - how bacteria survive protozoan grazing. Trends Microbiol. 13:302-307.
37. Ménard, L.-P., and J. D. Dubreuil. 2002. Enteroaggregative Escherichia coli heat-stable enterotoxin 1 (EAST1): a new toxin with an old twist. Crit. Rev. Microbiol. 28:43-60.
38. Mol, O., and B. Oudega. 1996. Molecular and structural aspects of fimbriae biosynthesis and assembly in Escherichia coli. FEMS Microbiol. Rev. 19:25-52.
39. Mühldorfer, I., G. Blum, A. Donohue-Rolfe, H. Heier, T. Ölschläger, H. Tschäpe, U. Wallner, and J. Hacker. 1996. Characterization of Escherichia coli strains isolated from environmental water habitats and from stool samples of healthy volunteers. Res. Microbiol. 147:625-635.
40. Niewerth, U., A. Frey, T. Voss, C. Le Bouguénec, G. Baljer, S. Franke, and M. A. Schmidt. 2001. The AIDA autotransporter system is associated with F18 and Stx2e in Escherichia coli isolates from pigs diagnosed with edema disease and postweaning diarrhea. Clin. Diagn. Lab. Immunol. 8:143-149.
41. Noamani, B. N., J. M. Fairbrother, and C. L. Gyles. 2003. Virulence genes of O149 enterotoxigenic Escherichia coli from outbreaks of postweaning diarrhea in pigs. Vet. Microbiol. 97:87-101.
42. Nougayrède, J.-P., S. Homburg, F. Taieb, M. Boury, E. Brzuszkiewicz, G. Gottschalk, C. Buchrieser, J. Hacker, U. Dobrindt, and E. Oswald. 2006. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 313:848-851.
43. Olasz, F., P. Z. Fekete, G. Blum-Oehler, Z. Boldogkoi, and B. Nagy. 2005. Characterization of an F18+ enterotoxigenic Escherichia coli strain from post weaning diarrhoea of swine, and of its conjugative virulence plasmid pTC. FEMS Microbiol. Lett. 244:281-289.
44. Osek, J. 2000. Virulence factors and genetic relatedness of Escherichia coli strains isolated from pigs with post-weaning diarrhea. Vet. Microbiol. 71:211-222.
45. Pachepsky, Y. A., A. M. Sadeghi, S. A. Bradford, D. R. Shelton, A. K. Guber, and T. Dao. 2006. Transport and fate of manure-borne pathogens: modeling perspective. Agric. Water Manag. 86:81-92.
46. Sapkota, A. R., F. C. Curriero, K. E. Gibson, and K. J. Schwab. 2007. Antibiotic-resistant enterococci and fecal indicators in surface water and groundwater impacted by a concentrated swine feeding operation. Environ. Health Perspect. 115:1040-1045.
47. Schouten, J. M., E. A. M. Graat, K. Frankena, A. W. Van De Giessen, W. K. Van Der Zwaluw, and M. C. M. De Jong. 2005. A longitudinal study of Escherichia coli O157 in cattle of a Dutch dairy farm and in the farm environment. Vet. Microbiol. 107:193-204.
48. Sonntag, A.-K., M. Bielaszewska, A. Mellmann, N. Dierksen, P. Schierack, L. H. Wieler, M. A. Schmidt, and H. Karch. 2005. Shiga toxin 2e-producing Escherichia coli isolates from humans and pigs differ in their virulence profiles and interactions with intestinal epithelial cells. Appl. Environ. Microbiol. 71:8855-8863.
49. Steinberg, K. M., and B. R. Levin. 2007. Grazing protozoa and the evolution of the Escherichia coli O157:H7 Shiga toxin-encoding prophage. Proc. Biol. Sci. 274:1921-1929.
50. Travis, R. M., C. L. Gyles, R. Reid-Smith, C. Poppe, S. A. McEwen, R. M. Friendship, N. Janecko, and P. Boerlin. 2006. Chloramphenicol and kanamycin resistance among porcine Escherichia coli in Ontario. J. Antimicrob. Chemother. 58:173-177.
51. Van Bochove, E., G. Thériault, F. Dechmi, M. L. Leclerc, and N. Goussard. 2007. Indicator of risk of water contamination by phosphorus: temporal trends for the province of Quebec from 1981 to 2001. Can. J. Soil Sci. 87:121-128.
52. Van den Broeck, W., E. Cox, B. Oudega, and B. M. Goddeeris. 2000. The F4 fimbrial antigen of Escherichia coli and its receptors. Vet. Microbiol. 71:223-244.
53. Versalovic, J., M. Schneider, F. J. De Bruijn, and J. R. Lupski. 1994. Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol. Cell. Biol. 5:25-40.