Abstract
One hundred and four enterotoxin producingEscherichia coli strains of wide geographical origin were tested for the expression of curli fimbriae by transmission electronmicroscopy and by ELISA using curli-specific antibodies, as well as for the presence of curli-specific gene sequences by PCR. All isolates, irrespective of the production of the fimbriae, carried sequences specific for the structure (csgA) and for one of the regulator genes (crl) of curli expression, respectively. Curli fimbriae were detected in 56 strains (53.8 %). Thirty-six strains expressed curli only when growing at 30 °C, 4 isolates were weakly curliated at 37 °C only, while on 16 strains curli was observed at both temperatures. On isolates carrying curli at both temperatures the expression of the fimbria was significantly stronger at 30 °C than at 37 °C. Curli proficiency significantly, but not completely, correlated with the binding of the Congo Red dye. The expression of curli did not confer epithelial cell invasiveness to ETEC strains but, once expressed at 30 °C, it facilitated the adherence of the bacteria to plastic surfaces. Curli present in more than half of the ETEC strains and expressed preferentially at low temperatures could be a factor facilitating the environmental survival of this food- and water-borne pathogen.
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References
Arnqvist A., Olsén A., Pfeifer J., Russell D.G., Normark S.: The Crl protein activates cryptic genes for curli formation and fibronectin binding inEscherichia coli HB101.Mol.Microbiol. 6, 2443–2452 (1992).
Arnqvist A., Olsén A., Normark S.: Sigma S-dependent growth-phase induction of theesgBA promoter inEscherichia coli can be achievedin vivo by σ 70 in the absence of the nucleoid-associated protein H-NS.Mol.Microbiol. 13, 1021–1032 (1994).
Austin J.W., Sanders G., Kay W.W., Collinson S.K.: Thin aggregative fimbriae enhanceSalmonella enteritidis biofilm formation.FEMS Microbiol.Lett. 162, 295–301 (1998).
Ben Nasr A., Olsen A., Sjöbring U., Muller-Esterl W., Bjorck L.: Assembly of human contact phase proteins and release of bradykinin at the surface of curli-expressingEscherichia coli.Mol.Microbiol. 20, 927–935 (1996).
Bian Z., Brauner A., Li Y., Normark S.: Expression of and cytokine activation byEscherichia coli curli fibers in human sepsis.J.Infect.Dis. 181, 602–612 (2000).
Bian Z., Yan Z.Q., Hansson G.K., Thoren P., Normark S.: Activation of inducible nitric oxide synthase/nitric oxide by curli fibers leads to a fall in blood pressure during systemicEscherichia coli infection in mice.J.Infect.Dis. 183, 612–619 (2001).
Christiansen G.D., Simpson W.A., Younger J.J., Baddour L.M., Barrett F.F., Melton D.M., Beachey E.H.: Adherence of coagulase negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices.J.Clin.Microbiol. 22, 996–1006 (1985).
Collinson S.K., Emödy L., Muller K.H., Trust T.J., Kay W.W.: Purification and characterization of thin, aggregative fimbriae fromSalmonella entertidis.J.Bacteriol. 173, 4773–4781 (1991).
Collinson S.K., Emödy L., Trust T.J., Kay W.W.: Thin aggregative fimbriae from diarrheagenicEscherichia coli.J.Bacteriol. 174, 4490–4495 (1992).
Collinson S.K., Doig P.C., Doran J.L., Clouthier S., Trust T.J., Kay W.W.: Thin, aggregative fimbriae mediate binding ofSalmonella enteritidis to fibronectin.J.Bacteriol. 175, 12–18 (1993).
Cookson A.L., Cooley W.A., Woodward M.J.: The role of type 1 and curli fimbriae of Shiga toxin-producingEscherichia coli in adherence to abiotic surfaces.Internat.J.Med.Microbiol. 292, 195–205 (2002).
Dibb-Fuller M.P., Allen-Vercoe E., Thorns C.J., Woodward M.J.: Fimbriae- and flagella-mediated association with and invasion of cultured epithelial cells bySalmonella enteritidis.Microbiology 145, 1023–1031 (1999).
Dworniczek E., Kuzko K., Mróz E., Wojciech L., Adamski R., Sobieszczańska B., Seniuk A.: Virulence factors andin vitro adherence ofEnterococcus strains to urinary catheters.Folia Microbiol. 48, 671–678 (2003).
Elsinghorst E.A., Kopecko D.J.: Molecular cloning of epithelial cell invasion determinants from enterotoxigenicEscherichia coli.Infect.Immun. 60, 2409–2417 (1992).
Evans D.G., Evans D.J. Jr.,Tjoa W.: Hemagglutination of human group A erythrocytes by enterotoxigenicEscherichia coli isolated from adults with diarrhea: correlation with colonization factor.Infect.Immun. 18, 330–337 (1977).
Franiczek R., Sobieszczańska B., Grabowski M., Mowszet K., Pytrus T.: Occurrence of extended-spectrum β-lactamases amongEscherichia coli isolates from hospitalized and healthy children.Folia Microbiol. 48, 243–248 (2003).
Gophna U., Barlev M., Seijffers R., Oelschlager T.A., Hacker J., Ron E.Z.: Curli fibers mediate internalization ofEscherichia coli by eukaryotic cells.Infect.Immun. 69, 2659–2665 (2001).
Grund S., Weber A.: A new type of fimbriae onSalmonella typhimurium.Zbl.Veterinarmed. B 35, 779–782 (1988).
Hammar M., Arnqvist A., Bian Z., Olsen A., Normark S.: Expression of twocsg operons is required for production of fibronectin-and Congo Red-binding curli polymers inEscherichia coli K-12.Mol.Microbiol. 18, 661–670 (1995).
Herwald H., Morgelin M., Olsen A., Rhen M., Dahlback B., Muller-Esterl W., Bjorck L.: Activation of the contact-phase system on bacterial surfaces — a clue to serious complications in infections diseases.Nature Med. 4, 298–302 (1998).
La Ragione R.M., Cooley W.A., Woodward M.J.: The role of fimbriae and flagella in the adherence of avian strains ofEscherichia coli O78:K80 to tissue culture cells and tracheal and gut explants.J.Med.Microbiol. 49, 327–238 (2000).
Liptáková A., Siegfried L., Podracka L., Sabol M., Sehnálkova H., Bogyiová E., Rosocha J., Kmeiová M., Kerestešová H., Kotulová D.: Detection of Shiga toxins, intimin and enterohemolysin inEscherichia coli strains isolated from children in eastern Slovakia.Folia Microbiol. 47, 185–188 (2002).
Maurelli A.T., Blackmon B., Curtiss R.: 3rd: Loss of pigmentation inShigella flexneri 2a is correlated with loss of virulence and virulence-associated plasmid.Infect.Immun. 43, 397–401 (1984).
Maurer J.J., Brown T.P., Steffens W.L., Thayer S.G.: The occurrence of ambient temperature-regulated adhesins. curli, and the temperature-sensitive hemagglutinin tsh among avianEscherichia coli.Avian Dis. 42, 106–118 (1998).
Nataro J.P., Kaper J.B.: DiarrheagenicEscherichia coli.Clin.Microbiol.Rev. 11, 142–201 (1998).
Olsen A., Jonsson A., Normark S.: Fibronectin binding mediated by a novel class of surface organelles onEscherichia coli.Nature 338, 652–655 (1989).
Olsén A., Arnqvist A., Hammar M., Sukupolvi S., Normark S.: The RpoS σ factor relieves H-NS-mediated transcriptional repression ofcsgA, the subunit gene of fibronectin-binding curli inEscherichia coli.Mol.Microbiol. 7, 523–536 (1993).
Olsen A., Wick M.J., Morgelin M., Bjorck L.: Curli, fibrous surface proteins ofEscherichia coli, interact with major histocompatibility complex class I molecules.Infect.Immun. 66, 944–949 (1998).
Pátri E., Szabó E., Pal T., Emödy L.: Thin aggregative fimbriae on urinaryEscherichia coli isolates.Adv.Exp.Med.Biol. 485, 219–224 (2000).
Provence D.L., Curhss R. 3rd: Role ofcrl in avian pathogenicEscherichia coli: a knockout mutation ofcrl does not affect hemagglutination activity, fibronectin binding, or curli production.Infect.Immun. 60, 4460–4467 (1992).
Reisner A., Haagensen J.A., Schembri M.A., Zechner E.L., Molin S.: Development and maturation ofEscherichia coli K-12 biofilms.Mol.Microbiol. 48, 933–946 (2003).
Romling U., Sierralta W.D., Eriksson K., Normark S.: Multicellular and aggregative behavior ofSalmonella typhimurium strains is controlled by mutations in theagfD promoter.Mol.Microbiol. 28, 249–264 (1998).
Sakellaris H., Hannink N.K., Rajakumar K., Bulach D., Hunt M., Sasakawa C., Adler B.: Curli loci ofShigella spp.Infect.Immun. 68, 3780–3783 (2000).
Sjöbring U., Pohl G., Olsen A.: Plasminogen, absorbed byEscherichia coli expressing curli or bySalmonella enteritidis expressing thin aggregative fimbriae, can be activated by simultaneously captured tissue-type plasminogen activator (t-PA).Mol.Microbiol. 14, 443–452 (1994).
Sobieszczanska B.M., Osek J.: Enteroaggregative and cell-detachingEscherichia coli strains among Polish children with and without diarrhea.Folia Microbiol. 48, 823–828 (2003).
Stacy-Phipps S., Mecca J.J., Weiss J.B.: Multiplex PCR assay and simple preparation method for stool specimens detect enterotoxigenicEscherichia coli DNA during course of infection.J.Clin.Microbiol. 33, 1054–1059 (1995).
Sukupolvi S., Lorenz R.G., Gordon J.I., Bian Z., Pfeifer J.D., Normark S.J., Rhen M.: Expression of thin aggregative fimbriae promotes interaction ofSalmonella typhimurium SR-11 with mouse small intestinal epithelial cells.Infect.Immun. 65, 5320–5325 (1997).
Surgalla M.J., Beesley E.D.: Congo red-agar plating medium for detecting pigmentation inPasteurella pestis.Appl.Microbiol. 18, 834–837 (1969).
Uhlich G.A., Keen J.E., Elder R.O.: Mutations in thecsgD promoter associated with variations in curli expression in certain strains ofEscherichia coli O157:H7.Appl.Environ.Microbiol. 67, 2367–2370 (2001).
Uhlich G.A., Keen J.E., Elder R.O.: Variations in thecsgD promoter ofEscherichia coli O157:H7 associated with increased virulence in mice and increased invasion of HEp-2 cells.Infect.Immun. 70, 395–399 (2002).
Vidal O., Longin R., Prigent-Combaret C., Dorel C., Hooreman M., Lejeune P.: Isolation of anEscherichia coli K-12 mutant strain able to form biofilms on inert surfaces: involvement of a newompR allele that increases curli expression.J.Bacteriol. 180, 2442–2449 (1998).
Vu-Khac H., Holoda E., Majerčiak M., Gašpar G., Pilipčinec E.: Genotyping of fimbrial adhesins inEscherichia coli strains isolated from Slovak piglets suffering from diarrhea.Folia Microbiol. 49, 59–63 (2004).
White A.P., Gibson D.L., Collinson S.K., Banser P.A., Kay W.W.: Extracellular polysaccharides associated with thin aggregative fimbriae ofSalmonella enterica serovar enteritidis.J.Bacteriol. 185, 5398–5407 (2003).
Zogaj X., Nimtz M., Rohde M., Bokranz W., Römling U.: The multicellular morphotypes ofSalmonella typhimarium andEscherichia coli produce cellulose as the second component of the extracellular matrix.Mol.Microbiol. 39, 1452–1463 (2001).
Zogaj X., Bokranz W., Nimtz M., Romling U.: Production of cellulose and curli fimbriae by members of the familyEnterobacteriaceae isolated from the human gastrointestinal tract.Infect.Immun. 71, 4151–4158 (2003).
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This work was supported by the grants NP/02/25 of theFaculty of Medicine and Health Sciences, University of the United Arab Emirates (Al Ain, United Arab Emirates) and by T030201 and T037833 of theNational Scientific Research foundation (OTKA), Hungary. The skillful technical assistance of Ms. C. Wéber is highly appreciated.
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Szabó, E., Skedsmo, A., Sonnevend, Á. et al. Curli expression of enterotoxigenicEscherichia coli . Folia Microbiol 50, 40–46 (2005). https://doi.org/10.1007/BF02931292
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DOI: https://doi.org/10.1007/BF02931292