Distinct acid resistance and survival fitness displayed by curli variants of enterohemorrhagic Escherichia coli O157:H7

Applied and Environmental Microbiology

Volumn 77, Issue 11, 2011, Pages 3685-3695

  Carter, Michelle Q ^a   Brandl, Maria T ^a   Louie, Jacqueline W ^a   Kyle, Jennifer L ^a   Carychao, Diana K ^a   Cooley, Michael B ^a   Parker, Craig T ^a   Bates, Anne H ^a   Mandrell, Robert E ^a  

^a WESTERN REGIONAL RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC ENVIRONMENT; BIOFILM FORMATION; CELL AGGREGATION; CELL POPULATIONS; CURLI PRODUCTION; DELETION MUTANTS; E.COLI O157:H7; ENTEROBACTERIACEAE; ENTEROHEMORRHAGIC ESCHERICHIA COLI; GROWTH CONDITIONS; NUTRIENT-LIMITED CONDITION; NUTRIENT-LIMITED ENVIRONMENT; OXYGEN DEPLETION; PARENTAL STRAINS; PHYSIOLOGICAL PROPERTIES; SURFACE ATTACHMENT;

CELL CULTURE; CELL PROLIFERATION; ESCHERICHIA COLI; NUTRIENTS; POPULATION STATISTICS;

ACID RESISTANCE;

ACID; BACTERIAL PROTEIN; CRL PROTEIN, BACTERIA;

ACID; ANIMAL; BIOFILM; CARBON; CELL ORGANELLE; COLIFORM BACTERIUM; CONCENTRATION (COMPOSITION); DEVELOPMENTAL BIOLOGY; FITNESS; ION; MUTATION; NUTRIENT LIMITATION; OXYGEN; POPULATION STRUCTURE; SURVIVAL;

ANIMAL; ANTIBIOTIC RESISTANCE; ARTICLE; DRUG EFFECT; ESCHERICHIA COLI O157; GENETIC VARIABILITY; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIAL VIABILITY; PHYSIOLOGY;

ACIDS; ANIMALS; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI O157; GENETIC VARIATION; HUMANS; MICROBIAL VIABILITY;

UNITED STATES;

ANIMALIA; ENTEROBACTERIACEAE; ESCHERICHIA COLI; SPINACIA OLERACEA;

EID: 79958270563     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02315-10     Document Type: Article

References (46)

1. Austin, J. W., G. Sanders, W. W. Kay, and S. K. Collinson. 1998. Thin aggregative fimbriae enhance Salmonella enteritidis biofilm formation. FEMS Microbiol. Lett. 162:295-301.
2. Avery, S. V. 2006. Microbial cell individuality and the underlying sources of heterogeneity. Nat. Rev. Microbiol. 4:577-587.
3. Barnhart, M. M., and M. R. Chapman. 2006. Curli biogenesis and function. Annu. Rev. Microbiol. 60:131-147.
4. Bian, Z., A. Brauner, Y. Li, and S. Normark. 2000. Expression of and cytokine activation by Escherichia coli curli fibers in human sepsis. J. Infect. Dis. 181:602-612.
5. Brzuszkiewicz, E., G. Gottschalk, E. Ron, J. Hacker, and U. Dobrindt. 2009. Adaptation of pathogenic E. coli to various niches: genome flexibility is the key. Genome Dyn. 6:110-125.
6. Casadaban, M. J. 1976. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and mu. J. Mol. Biol. 104:541-555.
7. Chapman, M. R., et al. 2002. Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295:851-855.
8. Cooley, M., et al. 2007. Incidence and tracking of Escherichia coli O157:H7 in a major produce production region in California. PLoS One 2:e1159.
9. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
10. Davidson, C. J., and M. G. Surette. 2008. Individuality in bacteria. Annu. Rev. Genet. 42:253-268.
11. Dorel, C., O. Vidal, C. Prigent-Combaret, I. Vallet, and P. Lejeune. 1999. Involvement of the Cpx signal transduction pathway of E. coli in biofilm formation. FEMS Microbiol. Lett. 178:169-175.
12. Ferrieres, L., and D. J. Clarke. 2003. The RcsC sensor kinase is required for normal biofilm formation in Escherichia coli K-12 and controls the expression of a regulon in response to growth on a solid surface. Mol. Microbiol. 50:1665-1682.
13. Foster, J. W. 2004. Escherichia coli acid resistance: tales of an amateur acidophile. Nat. Rev. Microbiol. 2:898-907.
14. Gophna, U., et al. 2001. Curli fibers mediate internalization of Escherichia coli by eukaryotic cells. Infect. Immun. 69:2659-2665.
15. Hammar, M., A. Arnqvist, Z. Bian, A. Olsen, and S. Normark. 1995. Expression of two csg operons is required for production of fibronectin- and Congo red-binding curli polymers in Escherichia coli K-12. Mol. Microbiol. 18:661-670.
16. Hammar, M., Z. Bian, and S. Normark. 1996. Nucleator-dependent intercellular assembly of adhesive curli organelles in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 93:6562-6566.
17. Hammer, N. D., J. C. Schmidt, and M. R. Chapman. 2007. The curli nucleator protein, CsgB, contains an amyloidogenic domain that directs CsgA polymerization. Proc. Natl. Acad. Sci. U. S. A. 104:12494-12499.
18. Hidalgo, G., X. Chen, A. G. Hay, and L. W. Lion. 2010. Curli produced by Escherichia coli PHL628 provide protection from Hg(II). Appl. Environ. Microbiol. 76:6939-6941.
19. Jubelin, G., et al. 2005. CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J. Bacteriol. 187:2038-2049.
20. Kai-Larsen, Y., et al. 2010. Uropathogenic Escherichia coli modulates immune responses and its curli fimbriae interact with the antimicrobial peptide LL-37. PLoS Pathog. 6:e1001010.
21. Keys, C., S. Kemper, and P. Keim. 2005. Highly diverse variable number tandem repeat loci in the E. coli O157:H7 and O55:H7 genomes for highresolution molecular typing. J. Appl. Microbiol. 98:928-940.
22. Khurana, R., V. N. Uversky, L. Nielsen, and A. L. Fink. 2001. Is Congo red an amyloid-specific dye? J. Biol. Chem. 276:22715-22721.
23. Kikuchi, T., Y. Mizunoe, A. Takade, S. Naito, and S. Yoshida. 2005. Curli fibers are required for development of biofilm architecture in Escherichia coli K-12 and enhance bacterial adherence to human uroepithelial cells. Microbiol. Immunol. 49:875-884.
24. Lindstedt, B. A., E. Heir, E. Gjernes, T. Vardund, and G. Kapperud. 2003. DNA fingerprinting of Shiga-toxin producing Escherichia coli O157 based on multiple-locus variable-number tandem-repeats analysis (MLVA). Ann. Clin. Microbiol. Antimicrob. 2:12.
25. Mandrell, R. E. 2009. Enteric human pathogens associated with fresh produce: sources, transport and ecology, p. 5-41. In X. Fan, B. A. Niemira, C. J. Doona, F. E. Feeherry, and R. B. Gravani (ed.), Microbial safety of fresh produce. IFT Press/Wiley-Blackwell Publishing, Ames, IA.
26. Manning, S. D., et al. 2008. Variation in virulence among clades of Escherichia coli O157:H7 associated with disease outbreaks. Proc. Natl. Acad. Sci. U. S. A. 105:4868-4873.
27. Maurer, J. J., T. P. Brown, W. L. Steffens, and S. G. Thayer. 1998. The occurrence of ambient temperature-regulated adhesins, curli, and the temperature-sensitive hemagglutinin tsh among avian Escherichia coli. Avian Dis. 42:106-118.
28. Olsen, A., A. Jonsson, and S. Normark. 1989. Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338:652-655.
29. O'Toole, G. A., and R. Kolter. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28:449-461.
30. Pratt, L. A., and T. J. Silhavy. 1998. Crl stimulates RpoS activity during stationary phase. Mol. Microbiol. 29:1225-1236.
31. Rangel, J. M., P. H. Sparling, C. Crowe, P. M. Griffin, and D. L. Swerdlow. 2005. Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982-2002. Emerg. Infect. Dis. 11:603-609.
32. Robinson, L. S., E. M. Ashman, S. J. Hultgren, and M. R. Chapman. 2006. Secretion of curli fibre subunits is mediated by the outer membrane-localized CsgG protein. Mol. Microbiol. 59:870-881.
33. Romling, U., W. D. Sierralta, K. Eriksson, and S. Normark. 1998. Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol. Microbiol. 28:249-264.
34. Smalley, J. W., A. J. Birss, A. S. McKee, and P. D. Marsh. 1995. Congo red binding by Porphyromonas gingivalis is mediated by a 66 kDa outer-membrane protein. Microbiology 141(Pt. 1):205-211.
35. Sommerfeldt, N., et al. 2009. Gene expression patterns and differential input into curli fimbriae regulation of all GGDEF/EAL domain proteins in Escherichia coli. Microbiology 155:1318-1331.
36. Szabo, E., et al 2005. Curli expression of enterotoxigenic Escherichia coli. Folia Microbiol. (Praha) 50:40-46.
37. Tagliabue, L., A. Maciag, D. Antoniani, and P. Landini. 2010. The yddV-dos operon controls biofilm formation through the regulation of genes encoding curli fibers' subunits in aerobically growing Escherichia coli. FEMS Immunol. Med. Microbiol. 59:477-484.
38. Tukel, C., et al. 2005. CsgA is a pathogen-associated molecular pattern of Salmonella enterica serotype Typhimurium that is recognized by Toll-like receptor 2. Mol. Microbiol. 58:289-304.
39. Uhlich, G. A., N. W. Gunther, D. O. Bayles, and D. A. Mosier. 2009. The CsgA and Lpp proteins of an Escherichia coli O157:H7 strain affect HEp-2 cell invasion, motility, and biofilm formation. Infect. Immun. 77:1543-1552.
40. Uhlich, G. A., J. E. Keen, and R. O. Elder. 2001. Mutations in the csgD promoter associated with variations in curli expression in certain strains of Escherichia coli O157:H7. Appl. Environ. Microbiol. 67:2367-2370.
41. Uhlich, G. A., J. E. Keen, and R. O. Elder. 2002. Variations in the csgD promoter of Escherichia coli O157:H7 associated with increased virulence in mice and increased invasion of HEp-2 cells. Infect. Immun. 70:395-399.
42. Vidal, O., et al. 1998. Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases curli expression. J. Bacteriol. 180:2442-2449.
43. Wang, X., and M. R. Chapman. 2008. Sequence determinants of bacterial amyloid formation. J. Mol. Biol. 380:570-580.
44. Westerman, R. B., Y. He, J. E. Keen, E. T. Littledike, and J. Kwang. 1997. Production and characterization of monoclonal antibodies specific for the lipopolysaccharide of Escherichia coli O157. J. Clin. Microbiol. 35:679-684.
45. White, A. P., et al. 2008. Aggregation via the red, dry, and rough morphotype is not a virulence adaptation in Salmonella enterica serovar Typhimurium. Infect. Immun. 76:1048-1058.
46. Zogaj, X., W. Bokranz, M. Nimtz, and U. Romling. 2003. Production of cellulose and curli fimbriae by members of the family Enterobacteriaceae isolated from the human gastrointestinal tract. Infect. Immun. 71:4151-4158.