Potentially pathogenic Escherichia coli can form a biofilm under conditions relevant to the food production chain

Applied and Environmental Microbiology

Volumn 80, Issue 7, 2014, Pages 2042-2049

  Nesse, Live L ^a   Sekse, Camilla ^a   Berg, Kristin ^a,b   Johannesen, Karianne C S ^a   Solheim, Heidi ^a   Vestby, Lene K ^a   Urdahl, Anne Margrete ^a  

^a NORWEGIAN VETERINARY INSTITUTE   (Norway)

^b Fish Vet Group Norge   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGES; BIOFILMS; ESCHERICHIA COLI; GENE ENCODING; HYDROPHOBICITY;

BACTERIAL CELLS; BIOFILM PRODUCTION; FOOD PRODUCTION; GENERAL CORRELATIONS; PATHOGENIC ESCHERICHIA COLI; SEROTYPES; THREE TEMPERATURE; VIRULENCE FACTORS;

FOOD MICROBIOLOGY;

BIOFILM; COLIFORM BACTERIUM; FOOD PRODUCTION; HYDROPHOBICITY; PATHOGENICITY; TEMPERATURE EFFECT; VIRULENCE;

ADHESIN; EAEA PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; GLASS; POLYSTYRENE DERIVATIVE; SHIGA TOXIN; STAINLESS STEEL;

ANIMAL; ARTICLE; BACTERIOPHAGE; BACTERIUM ADHERENCE; BIOFILM; CHEMICAL PHENOMENA; CHEMISTRY; ESCHERICHIA COLI; FECES; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MICROBIOLOGY; PHYSICAL CHEMISTRY; PHYSIOLOGY; SEROTYPING; SHEEP; SURFACE PROPERTY; TEMPERATURE;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL ADHESION; BACTERIOPHAGES; BIOFILMS; ENVIRONMENTAL MICROBIOLOGY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FECES; GLASS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; PHYSICOCHEMICAL PHENOMENA; POLYSTYRENES; SEROTYPING; SHEEP; SHIGA TOXIN; STAINLESS STEEL; SURFACE PROPERTIES; TEMPERATURE;

EID: 84896057334     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03331-13     Document Type: Article

References (46)

1. Paton JC, Paton AW. 1998. Pathogenesis and diagnosis of Shiga toxinproducing Escherichia coli infections. Clin. Microbiol. Rev. 11:450-479.
2. Karmali MA. 2004. Infection by Shiga toxin-producing Escherichia coli: an overview. Mol. Biotechnol. 26:117-122. http://dx.doi.org/10.1385 /MB:26:2:117.
3. Girard F, Batisson I, Frankel GM, Harel J, Fairbrother JM. 2005. Interaction of enteropathogenic and Shiga toxin-producing Escherichia coli and porcine intestinal mucosa: role of intimin and Tir in adherence. Infect. Immun. 73:6005-6016. http://dx.doi.org/10.1128/IAI.73.9.6005-6016.2005.
4. Tzipori S, Gunzer F, Donnenberg MS, de Montigny L, Kaper JB, Donohue-Rolfe A. 1995. The role of the eaeA gene in diarrhea and neurological complications in a gnotobiotic piglet model of enterohemorrhagic Escherichia coli infection. Infect. Immun. 63:3621-3627.
5. Fitzhenry RJ, Pickard DJ, Hartland EL, Reece S, Dougan G, Phillips AD, Frankel G. 2002. Intimin type influences the site of human intestinal mucosal colonisation by enterohaemorrhagic Escherichia coli O157:H7. Gut 50:180-185. http://dx.doi.org/10.1136/gut.50.2.180.
6. Mundy R, Schuller S, Girard F, Fairbrother JM, Phillips AD, Frankel G. 2007. Functional studies of intimin in vivo and ex vivo: implications for host specificity and tissue tropism. Microbiology 153:959-967. http://dx .doi.org/10.1099/mic.0.2006/003467-0.
7. Shaikh N, Tarr PI. 2003. Escherichia coli O157:H7 Shiga toxin-encoding bacteriophages: integrations, excisions, truncations, and evolutionary implications. J. Bacteriol. 185:3596-3605. http://dx.doi.org/10.1128/JB.185 .12.3596-3605.2003.
8. Brooks JT, Sowers EG, Wells JG, Greene KD, Griffin PM, Hoekstra RM, Strockbine NA. 2005. Non-O157 Shiga toxin-producing Escherichia coli infections in the United States, 1983-2002. J. Infect. Dis. 192:1422-1429. http://dx.doi.org/10.1086/466536.
9. Bielaszewska M, Kock R, Friedrich AW, von Eiff C, Zimmerhackl LB, Karch H, Mellmann A. 2007. Shiga toxin-mediated hemolytic uremic syndrome: time to change the diagnostic paradigm? PLoS One 2:e1024. http://dx.doi.org/10.1371/journal.pone.0001024.
10. Hofshagen M, Lange H, Hauge K. 2011. Trends and source of zoonoses and zoonotic agents in humans foodstuffs, animals and feedingstuffs. Norwegian Veterinary Institute, Oslo, Norway. http://www.vetinst.no /eng/Publications/Zoonosis-Reports/Zoonosis-report-2011.
11. Schimmer B, Nygard K, Eriksen HM, Lassen J, Lindstedt BA, Brandal LT, Kapperud G, Aavitsland P. 2008. Outbreak of haemolytic uraemic syndrome in Norway caused by stx2-positive Escherichia coli O103:H25 traced to cured mutton sausages. BMC Infect. Dis. 8:41. http://dx.doi.org /10.1186/1471-2334-8-41.
12. Sekse C, O'Sullivan K, Granum PE, Rorvik LM, Wasteson Y, Jorgensen HJ. 2009. An outbreak of Escherichia coli O103:H25-bacteriological investigations and genotyping of isolates from food. Int. J. Food Microbiol. 133:259-264. http://dx.doi.org/10.1016/j.ijfoodmicro.2009.05.026.
13. Chmielewski RAN, Frank JF. 2003. Biofilm formation and control in food processing facilities. Comp. Rev. Food Sci. Technol. 2:22-32. http: //dx.doi.org/10.1111/j.1541-4337.2003.tb00012.x.
14. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49:711-745. http: //dx.doi.org/10.1146/annurev.mi.49.100195.003431.
15. Zogaj X, Nimtz M, Rohde M, Bokranz W, Romling U. 2001. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the secondcomponentof the extracellular matrix. Mol. Microbiol. 39:1452-1463. http://dx.doi.org/10.1046/j.1365-2958.2001.02337.x.
16. Vestby LK, Moretro T, Ballance S, Langsrud S, Nesse LL. 2009. Survival potential of wild type cellulose deficient Salmonella from the feed industry. BMC Vet. Res. 5:43. http://dx.doi.org/10.1186/1746-6148-5-43.
17. Moretro T, Vestby LK, Nesse LL, Storheim S, Kotlarz K, Langsrud S. 2009. Evaluation of efficacy of disinfectants against Salmonella from the feed industry. J. Appl. Microbiol. 106:1005-1012. http://dx.doi.org/10 .1111/j.1365-2672.2008.04067.x.
18. Vestby LK, Moretro T, Langsrud S, Heir E, Nesse LL. 2009. Biofilm forming abilities of Salmonella are correlated with persistence in fish meal and feed factories. BMC Vet. Res. 5:20. http://dx.doi.org/10.1186/1746 -6148-5-20.
19. Møretrø T, Langsrud S. 2004. Listeria monocytogenes: biofilm formation and persistence in food-processing environments. Biofilms 1:107-121. http://dx.doi.org/10.1017/S1479050504001322.
20. Solheim HT, Sekse C, Urdahl AM, Wasteson Y, Nesse LL. 2013. Biofilm as an environment for dissemination of stx genes by transduction. Appl. Environ. Microbiol. 79:896-900. http://dx.doi.org/10.1128/AEM.03512-12.
21. Sekse C, Sunde M, Lindstedt BA, Hopp P, Bruheim T, Cudjoe KS, Kvitle B, Urdahl AM. 2011. Potentially human-pathogenic Escherichia coli O26 in Norwegian sheep flocks. Appl. Environ. Microbiol. 77:4949-4958. http://dx.doi.org/10.1128/AEM.00189-11.
22. Sekse C, Sunde M, Hopp P, Bruheim T, Cudjoe KS, Kvitle B, Urdahl AM. 2013. Low prevalence of Shiga toxin-producing Escherichia coli O103 in Norwegian sheep flocks. Appl. Environ. Microbiol. 79:7502-7509. http: //dx.doi.org/10.1128/AEM.01825-13.
23. Zhang WL, Kohler B, Oswald E, Beutin L, Karch H, Morabito S, Caprioli A, Suerbaum S, Schmidt H. 2002. Genetic diversity of intimin genes of attaching and effacing Escherichia coli strains. J. Clin. Microbiol. 40:4486-4492. http://dx.doi.org/10.1128/JCM.40.12.4486-4492.2002.
24. Blanco M, Blanco JE, Mora A, Dahbi G, Alonso MP, Gonzalez EA, Bernardez MI, Blanco J. 2004. Serotypes, virulence genes, and intimin types of Shiga toxin (verotoxin)-producing Escherichia coli isolates from cattle in Spain and identification of a new intimin variant gene (eae-ξ). J. Clin. Microbiol. 42:645-651. http://dx.doi.org/10.1128/JCM.42.2.645 -651.2004.
25. Sekse C, Muniesa M, Wasteson Y. 2008. Conserved Stx2 phages from Escherichia coli O103:H25 isolated from patients suffering from hemolytic uremic syndrome. Foodborne Pathog. Dis. 5:801-810. http://dx.doi.org /10.1089/fpd.2008.0130.
26. Mattos-Guaraldi AL, Formiga LC, Andrade AF. 1999. Cell surface hydrophobicity of sucrose fermenting and nonfermenting Corynebacterium diphtheriae strains evaluated by different methods. Curr. Microbiol. 38: 37-42. http://dx.doi.org/10.1007/PL00006769.
27. Di Bonaventura G, Piccolomini R, Paludi D, D'Orio V, Vergara A, Conter M, Ianieri A. 2008. Influence of temperature on biofilm formation by Listeria monocytogenes on various food-contact surfaces: relationship with motility and cell surface hydrophobicity. J. Appl. Microbiol. 104:1552-1561. http://dx.doi.org/10.1111/j.1365-2672.2007.03688.x.
28. Norwood DE, Gilmour A. 1999. Adherence of Listeria monocytogenes strains to stainless steel coupons. J. Appl. Microbiol. 86:576-582. http://dx .doi.org/10.1046/j.1365-2672.1999.00694.x.
29. Schonewille E, Nesse LL, Hauck R, Windhorst D, Hafez HM, Vestby LK. 2012. Biofilm building capacity of Salmonella enterica strains from the poultry farm environment. FEMS Immunol. Med. Microbiol. 65:360-365. http://dx.doi.org/10.1111/j.1574-695X.2012.00966.x.
30. Martinez-Medina M, Naves P, Blanco J, Aldeguer X, Blanco JE, Blanco M, Ponte C, Soriano F, Darfeuille-Michaud A, Garcia-Gil LJ. 2009. Biofilm formation as a novel phenotypic feature of adherent-invasive Escherichia coli (AIEC). BMC Microbiol. 9:202. http://dx.doi.org/10.1186 /1471-2180-9-202.
31. Wang R, Bono JL, Kalchayanand N, Shackelford S, Harhay DM. 2012. Biofilm formation by Shiga toxin-producing Escherichia coli O157:H7 and non-O157 strains and their tolerance to sanitizers commonly used in the food processing environment. J. Food Prot. 75:1418-1428. http://dx.doi .org/10.4315/0362-028X.JFP-11-427.
32. Cremet L, Corvec S, Bemer P, Bret L, Lebrun C, Lesimple B, Miegeville AF, Reynaud A, Lepelletier D, Caroff N. 2012. Orthopaedic-implant infections by Escherichia coli: molecular and phenotypic analysis of the causative strains. J. Infect. 64:169-175. http://dx.doi.org/10.1016/j.jinf .2011.11.010.
33. Salo J, Sevander JJ, Tapiainen T, Ikaheimo I, Pokka T, Koskela M, Uhari M. 2009. Biofilm formation by Escherichia coli isolated from patients with urinary tract infections. Clin. Nephrol. 71:501-507. http://dx .doi.org/10.5414/CNP71501.
34. Reisner A, Krogfelt KA, Klein BM, Zechner EL, Molin S. 2006. In vitro biofilm formation of commensal and pathogenic Escherichia coli strains: impact of environmental and genetic factors. J. Bacteriol. 188:3572-3581. http://dx.doi.org/10.1128/JB.188.10.3572-3581.2006.
35. Goulter RM, Gentle IR, Dykes GA. 2009. Issues in determining factors influencing bacterial attachment: a review using the attachment of Escherichia coli to abiotic surfaces as an example. Lett. Appl. Microbiol. 49:1-7. http://dx.doi.org/10.1111/j.1472-765X.2009.02591.x.
36. Rosenberg M, Blumberger Y, Judes H, Bar-Ness R, Rubinstein E, Mazor Y. 1986. Cell surface hydrophobicity of pigmented and nonpigmented clinical Serratia marcescens strains. Infect. Immun. 51:932-935.
37. Yousefi Rad AY, Ayhan H, Piskin E. 1998. Adhesion of different bacterial strains to low-temperature plasma-treated sutures. J. Biomed. Mater. Res. 41:349-358. http://dx.doi.org/10.1002/(SICI)1097-4636(19980905)41:3349::AID-JBM23.0.CO;2-C.
38. Liu Y, Yang SF, Li Y, Xu H, Qin L, Tay JH. 2004. The influence of cell and substratum surface hydrophobicities on microbial attachment. J. Biotechnol. 110:251-256. http://dx.doi.org/10.1016/j.jbiotec.2004.02.012.
39. Abban S, Jakobsen M, Jespersen L. 2012. Attachment behaviour of Escherichia coli K12 and Salmonella Typhimurium P6 on food contact surfaces for food transportation. Food Microbiol. 31:139-147. http://dx .doi.org/10.1016/j.fm.2012.04.003.
40. Zita A, Hermansson M. 1997. Effects of bacterial cell surface structures and hydrophobicity on attachment to activated sludge flocs. Appl. Environ. Microbiol. 63:1168-1170.
41. Li J, McLandsborough LA. 1999. The effects of the surface charge and hydrophobicity of Escherichia coli on its adhesion to beef muscle. Int. J. Food Microbiol. 53:185-193. http://dx.doi.org/10.1016/S0168-1605 (99)00159-2.
42. Hassan AN, Frank JF. 2004. Attachment of Escherichia coli O157:H7 grown in tryptic soy broth and nutrient broth to apple and lettuce surfaces as related to cell hydrophobicity, surface charge, and capsule production. Int. J. Food Microbiol. 96:103-109. http://dx.doi.org/10.1016/S0168-1605 (03)00160-0.
43. Rivas L, Fegan N, Dykes GA. 2007. Attachment of Shiga toxigenic Escherichia coli to stainless steel. Int. J. Food Microbiol. 115:89-94. http://dx .doi.org/10.1016/j.ijfoodmicro.2006.10.027.
44. Beloin C, Roux A, Ghigo JM. 2008. Escherichia coli biofilms. Curr. Top. Microbiol. Immunol. 322:249-289. http://europepmc.org/articles/PMC2 864707;jsessionid=AHnDJOcAmVOgt5A9ugrr.0.
45. Farfan MJ, Torres AG. 2012. Molecular mechanisms that mediate colonization of Shiga toxin-producing Escherichia coli strains. Infect. Immun. 80:903-913. http://dx.doi.org/10.1128/IAI.05907-11.
46. Umanski T, Rosenshine I, Friedberg D. 2002. Thermoregulated expression of virulence genes in enteropathogenic Escherichia coli. Microbiology 148:2735-2744. http://mic.sgmjournals.org/content/148/9/2735.long.