1,203
Views
1
CrossRef citations to date
0
Altmetric
Research Paper

Abundant production of exopolysaccharide by EAEC strains enhances the formation of bacterial biofilms in contaminated sprouts

, , ORCID Icon, , , , & show all
Pages 264-278 | Received 17 Aug 2017, Accepted 12 Jan 2018, Published online: 19 Apr 2018

References

  • Nataro JP, Steiner T, Guerrant RL. Enteroaggregative Escherichia coli. Emerg Infect Dis. 1998;4:251–61. doi:10.3201/eid0402.980212.
  • Dallman TJ, Chattaway MA, Cowley LA, Doumith M, Tewolde R, Wooldridge DJ, Underwood A, Ready D, Wain J, Foster K, et al. An investigation of the diversity of strains of enteroaggregative Escherichia coli isolated from cases associated with a large multi-pathogen foodborne outbreak in the UK. PLoS One. 2014;9:e98103. doi:10.1371/journal.pone.0098103.
  • Nataro JP. Outbreak of hemolytic-uremic syndrome linked to Shiga toxin-producing enteroaggregative Escherichia coli O104:H4. Pediatr Res 2011;70:221. doi:10.1203/PDR.0b013e31822d5ce9.
  • Rasko DA, Webster DR, Sahl JW, Bashir A, Boisen N, Scheutz F, Paxinos EE, Sebra R, Chin CS, Iliopoulos D, et al. Origins of the E. coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. N Engl J Med. 2011;365:709–17. doi:10.1056/NEJMoa1106920.
  • Scharlach M, Diercke M, Dreesman J, Jahn N, Krieck M, Beyrer K, Claußen K, Pulz M, Floride R. Epidemiological analysis of a cluster within the outbreak of Shiga toxin-producing Escherichia coli serotype O104:H4 in Northern Germany, 2011. Int J Hyg Environ Health. 2013;216:341–5. doi:10.1016/j.ijheh.2012.10.001.
  • Buchholz U, Bernard H, Werber D, Böhmer MM, Remschmidt C, Wilking H, Deleré Y, an der Heiden M, Adlhoch C, Dreesman J, et al. German outbreak of Escherichia coli O104:H4 associated with sprouts. N Engl J Med. 2011;365:1763–70. doi:10.1056/NEJMoa1106482.
  • Knodler M, Berger M, Dobrindt U. Long-term survival of the Shiga toxin-producing Escherichia coli O104:H4 outbreak strain on fenugreek seeds. Food Microbiol. 2016;59:190–5. doi:10.1016/j.fm.2016.06.005.
  • King LA, Nogareda F, Weill FX, Mariani-Kurkdjian P, Loukiadis E, Gault G, Jourdan-DaSilva N, Bingen E, Macé M, Thevenot D, et al. Outbreak of Shiga toxin-producing Escherichia coli O104:H4 associated with organic fenugreek sprouts, France, June 2011. Clin Infect Dis. 2012;54:1588–94. doi:10.1093/cid/cis255.
  • Nataro JP, Yikang D, Yingkang D, Walker K. AggR, a transcriptional activator of aggregative adherence fimbria I expression in enteroaggregative Escherichia coli. J Bacteriol. 1994;176:4691–9. doi:10.1128/jb.176.15.4691-4699.1994.
  • Morin N, Santiago AE, Ernst RK, Guillot SJ, Nataro JP. Characterization of the AggR regulon in enteroaggregative Escherichia coli. Infect Immun. 2013;81:122–32. doi:10.1128/IAI.00676-12.
  • Dudley EG, Thomson NR, Parkhill J, Morin NP, Nataro JP. Proteomic and microarray characterization of the AggR regulon identifies a pheU pathogenicity island in enteroaggregative Escherichia coli. Mol Microbiol. 2006;61:1267–82. doi:10.1111/j.1365-2958.2006.05281.x.
  • Nishi J, Sheikh J, Mizuguchi K, Luisi B, Burland V, Boutin A, Rose DJ, Blattner FR, Nataro JP. The export of coat protein from enteroaggregative Escherichia coli by a specific ATP-binding cassette transporter system. J Biol Chem. 2003;278:45680–9. doi:10.1074/jbc.M306413200.
  • Sheikh J, Czeczulin JR, Harrington S, Hicks S, Henderson IR, Le Bouguénec C, Gounon P, Phillips A, Nataro JP. A novel dispersin protein in enteroaggregative Escherichia coli. J Clin Invest 2002;110:1329–37. doi:10.1172/JCI16172.
  • Harrington SM, Sheikh J, Henderson IR, Ruiz-Perez F, Cohen PS, Nataro JP. The Pic protease of enteroaggregative Escherichia coli promotes intestinal colonization and growth in the presence of mucin. Infect Immun. 2009;77:2465–73. doi:10.1128/IAI.01494-08.
  • Boisen N, Scheutz F, Rasko DA, Redman JC, Persson S, Simon J, Kotloff KL, Levine MM, Sow S, Tamboura B, et al. Genomic characterization of enteroaggregative Escherichia coli from children in Mali. J Infect Dis. 2012;205:431–44. doi:10.1093/infdis/jir757.
  • Ruiz-Perez F, Henderson IR, Leyton DL, Rossiter AE, Zhang Y, Nataro JP. Roles of periplasmic chaperone proteins in the biogenesis of serine protease autotransporters of Enterobacteriaceae. J Bacteriol. 2009;191:6571–83. doi:10.1128/JB.00754-09.
  • Ruiz-Perez F, Wahid R, Faherty CS, Kolappaswamy K, Rodriguez L, Santiago A, Murphy E, Cross A, Sztein MB, Nataro JP. Serine protease autotransporters from Shigella flexneri and pathogenic Escherichia coli target a broad range of leukocyte glycoproteins. Proc Natl Acad Sci U S A. 2011;108:12881–6. doi:10.1073/pnas.1101006108.
  • Koo H, Xiao J, Klein MI. Extracellular polysaccharides matrix–an often forgotten virulence factor in oral biofilm research. Int J Oral Sci. 2009;1:229–34. doi:10.4248/IJOS.09086.
  • Adcox HE, Vasicek EM, Dwivedi V, Hoang KV, Turner J, Gunn JS. Salmonella Extracellular Matrix Components Influence Biofilm Formation and Gallbladder Colonization. Infect Immun. 2016;84:3243–51. doi:10.1128/IAI.00532-16.
  • Jann K, Jann B. Capsules of Escherichia coli, expression and biological significance. Can J Microbiol. 1992;38:705–10. doi:10.1139/m92-116.
  • Berk SL, Neumann P, Holtsclaw S, Smith JK. Escherichia coli pneumonia in the elderly with reference to the role of E. coli K1 capsular polysaccharide antigen. Am J Med. 1982;72:899–902. doi:10.1016/0002-9343(82)90849-X.
  • Cross AS, Gemski P, Sadoff JC, Orskov F, Orskov I. The importance of the K1 capsule in invasive infections caused by Escherichia coli. J Infect Dis. 1984;149:184–93. doi:10.1093/infdis/149.2.184.
  • Boulnois GJ, Roberts IS, Hodge R, Hardy KR, Jann KB, Timmis KN. Analysis of the K1 capsule biosynthesis genes of Escherichia coli: definition of three functional regions for capsule production. Mol Gen Genet. 1987;208:242–6. doi:10.1007/BF00330449.
  • Whitfield C. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem. 2006;75:39–68. doi:10.1146/annurev.biochem.75.103004.142545.
  • Whitfield C, Roberts IS. Structure, assembly and regulation of expression of capsules in Escherichia coli. Mol Microbiol 1999;31:1307–19. doi:10.1046/j.1365-2958.1999.01276.x.
  • Grant WD, Sutherland IW, Wilkinson JF. Exopolysaccharide colanic acid and its occurrence in the Enterobacteriaceae. J Bacteriol. 1969;100:1187–93.
  • Sutherland IW. The structure of colanic acid. J Gen Microbiol. 1969;57:18.
  • Reeves PP, Wang L. Genomic organization of LPS-specific loci. Curr Top Microbiol Immunol. 2002;264:109–35.
  • Preston A, Mandrell RE, Gibson BW, Apicella MA. The lipooligosaccharides of pathogenic gram-negative bacteria. Crit Rev Microbiol. 1996;22:139–80. doi:10.3109/10408419609106458.
  • Whitfield C, Kaniuk N, Frirdich E. Molecular insights into the assembly and diversity of the outer core oligosaccharide in lipopolysaccharides from Escherichia coli and Salmonella. J Endotoxin Res. 2003;9:244–9. doi:10.1177/09680519030090040501.
  • Jann K, Jann B. Polysaccharide antigens of Escherichia coli. Rev Infect Dis. 1987;9 Suppl 5:S517–26. doi:10.1093/clinids/9.Supplement_5.S517.
  • Chaudhuri RR, Sebaihia M, Hobman JL, Webber MA, Leyton DL, Goldberg MD, Cunningham AF, Scott-Tucker A, Ferguson PR, Thomas CM, et al. Complete genome sequence and comparative metabolic profiling of the prototypical enteroaggregative Escherichia coli strain 042. PLoS One. 2010;5:e8801. doi:10.1371/journal.pone.0008801.
  • Stevenson G, Lan R, Reeves PR. The colanic acid gene cluster of Salmonella enterica has a complex history. FEMS Microbiol Lett. 2000;191:11–6. doi:10.1111/j.1574-6968.2000.tb09312.x.
  • Stevenson G, Andrianopoulos K, Hobbs M, Reeves PR. Organization of the Escherichia coli K-12 gene cluster responsible for production of the extracellular polysaccharide colanic acid. J Bacteriol. 1996;178:4885–93. doi:10.1128/jb.178.16.4885-4893.1996.
  • Lopez-Torres AJ, Stout V. Role of colanic acid polysaccharide in serum resistance in vivo and in adherence. Curr Microbiol. 1996;33:383–9. doi:10.1007/s002849900132.
  • Mao Y, Doyle MP, Chen J. Insertion mutagenesis of wca reduces acid and heat tolerance of enterohemorrhagic Escherichia coli O157:H7. J Bacteriol. 2001;183:3811–5. doi:10.1128/JB.183.12.3811-3815.2001.
  • Mao Y, Doyle MP, Chen J. Role of colanic acid exopolysaccharide in the survival of enterohaemorrhagic Escherichia coli O157:H7 in simulated gastrointestinal fluids. Lett Appl Microbiol. 2006;42:642–7.
  • Danese PN, Pratt LA, Kolter R. Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J Bacteriol. 2000;182:3593–6. doi:10.1128/JB.182.12.3593-3596.2000.
  • Domka J, Lee J, Bansal T, Wood TK. Temporal gene-expression in Escherichia coli K-12 biofilms. Environ Microbiol. 2007;9:332–46. doi:10.1111/j.1462-2920.2006.01143.x.
  • Nataro JP, Deng Y, Cookson S, Cravioto A, Savarino SJ, Guers LD, Levine MM, Tacket CO. Heterogeneity of enteroaggregative Escherichia coli virulence demonstrated in volunteers. J Infect Dis. 1995;171:465–8. doi:10.1093/infdis/171.2.465.
  • Eslava C, Navarro-Garcia F, Czeczulin JR, Henderson IR, Cravioto A, Nataro JP. Pet, an autotransporter enterotoxin from enteroaggregative Escherichia coli. Infect Immun. 1998;66:3155–63.
  • Vial PA, Robins-Browne R, Lior H, Prado V, Kaper JB, Nataro JP, Maneval D, Elsayed A, Levine MM. Characterization of enteroadherent-aggregative Escherichia coli, a putative agent of diarrheal disease. J Infect Dis. 1988;158:70–9. doi:10.1093/infdis/158.1.70.
  • Olesen B, Neimann J, Bottiger B, Ethelberg S, Schiellerup P, Jensen C, Helms M, Scheutz F, Olsen KE, Krogfelt K, et al. Etiology of diarrhea in young children in Denmark: a case-control study. J Clin Microbiol. 2005;43:3636–41. doi:10.1128/JCM.43.8.3636-3641.2005.
  • Itoh Y, Nagano I, Kunishima M, Ezaki T. Laboratory investigation of enteroaggregative Escherichia coli O untypeable:H10 associated with a massive outbreak of gastrointestinal illness. J Clin Microbiol. 1997;35:2546–50.
  • Bernier C, Gounon P, Le Bouguenec C. Identification of an aggregative adhesion fimbria (AAF) type III-encoding operon in enteroaggregative Escherichia coli as a sensitive probe for detecting the AAF-encoding operon family. Infect Immun. 2002;70:4302–11. doi:10.1128/IAI.70.8.4302-4311.2002.
  • Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, Bidet P, Bingen E, Bonacorsi S, Bouchier C, Bouvet O, et al. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet. 2009;5:e1000344. doi:10.1371/journal.pgen.1000344.
  • Mathewson JJ, Oberhelman RA, Dupont HL, Javier de la Cabada F, Garibay EV. Enteroadherent Escherichia coli as a cause of diarrhea among children in Mexico. J Clin Microbiol. 1987;25:1917–9.
  • Cobeljic M, Miljkovic-Selimovic B, Paunovic-Todosijevic D, Velicković Z, Lepsanović Z, Zec N, Savić D, Ilić R, Konstantinović S, Jovanović B, et al. Enteroaggregative Escherichia coli associated with an outbreak of diarrhoea in a neonatal nursery ward. Epidemiol Infect. 1996;117:11–6. doi:10.1017/S0950268800001072.
  • Nataro JP, Baldini MM, Kaper JB, Black RE, Bravo N, Levine MM. Detection of an adherence factor of enteropathogenic Escherichia coli with a DNA probe. J Infect Dis. 1985;152:560–5. doi:10.1093/infdis/152.3.560.
  • Nwodo UU, Green E, Okoh AI. Bacterial exopolysaccharides: functionality and prospects. Int J Mol Sci. 2012;13:14002–15. doi:10.3390/ijms131114002.
  • Baranzoni GM, Fratamico PM, Rubio F, Glaze T, Bagi LK, Albonetti S. Detection and isolation of Shiga toxin-producing Escherichia coli (STEC) O104 from sprouts. Int J Food Microbiol. 2014;173:99–104. doi:10.1016/j.ijfoodmicro.2013.12.020.
  • Centers for Disease C, Prevention. Outbreak of Escherichia coli O104:H4 infections associated with sprout consumption – Europe and North America, May-July 2011. MMWR Morb Mortal Wkly Rep. 2013;62:1029–31.
  • Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A. 2000;97:6640–5. doi:10.1073/pnas.120163297.
  • Santiago AE, Ruiz-Perez F, Jo NY, Vijayakumar V, Gong MQ, Nataro JP. A large family of antivirulence regulators modulates the effects of transcriptional activators in Gram-negative pathogenic bacteria. PLoS Pathog. 2014;10:e1004153. doi:10.1371/journal.ppat.1004153.
  • Oxley D, Currie G, Bacic A. Monosaccharide analysis by methanolysis. CSH Protoc. 2006;2006(1):11.
  • Scott RW, Moore WE, Effland MJ, Millett MA. Ultraviolet spectrophotometric determination of hexoses, pentoses, and uronic acids after their reactions with concentrated sulfuric acid. Anal Biochem. 1967;21:68–80. doi:10.1016/0003-2697(67)90084-X.
  • Thibert RJ, Mazzuchin A. Study of sugars with cysteine–sulfuric acid reagents. Can J Biochem. 1969;47:203–6. doi:10.1139/o69-031.
  • Fassel TA, Mozdziak PE, Sanger JR, Edmiston CE. Superior preservation of the staphylococcal glycocalyx with aldehyde-ruthenium red and select lysine salts using extended fixation times. Microsc Res Tech. 1998;41:291–7. doi:10.1002/(SICI)1097-0029(19980515)41:4%3c291::AID-JEMT2%3e3.0.CO;2-U.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.