Colicin FY is a plasmid encoded toxin that recognizes a yersinia-specific outer membrane protein (YiuR) as a receptor molecule. We have previously shown that the activity spectrum of colicin FY comprises strains of the genus Yersinia. In this study, we analyzed the activity of colicin FY against 110 Yersinia enterocolitica isolates differing in geographical origin and source. All isolates were characterized through analysis of 16S rRNA genes, serotyping, biotyping, restriction profiling of genomic DNA, detection of virulence markers and susceptibility to antibiotics. This confirmed the broad variability of the collection, in which all 110 Y. enterocolitica isolates, representing 77 various strains, were inhibited by colicin FY. Although isolates showed variable levels of susceptibility to colicin FY, it was not associated with any strain characteristic. The universal susceptibility of Y. enterocolitica strains to colicin FY together with the absence of activity towards strains outside the Yersinia genus suggests potential therapeutic applications for colicin FY.

Department of Biology Faculty of Medicine Masaryk University Brno Czech Republic

See more in PubMed

Aleksić S, Bockemühl J (1984) Proposed revision of the Wauters et al. antigenic scheme for serotyping of Yersinia enterocolitica . J Clin Microbiol 20: 99–102. PubMed PMC

Wauters G, Kandolo K, Janssens M (1987) Revised biogrouping scheme of Yersinia enterocolitica . Contrib Microbiol Immunol 9: 14–21. PubMed

Wauters G, Aleksić S, Charlier J, Schulze G (1991) Somatic and flagellar antigens of Yersinia enterocolitica and related species. Contrib Microbiol Immunol 12: 239–243. PubMed

Bottone EJ (1997) Yersinia enterocolitica: the charisma continues. Clin Microbiol Rev 10: 257–276. PubMed PMC

Bottone EJ (1999) Yersinia enterocolitica: overview and epidemiologic correlates. Microbes and Infection 1: 323–333. PubMed

Fredriksson-Ahomaa M, Hallanvuo S, Korte T, Siitonen A, Korkeala H (2001) Correspondence of genotypes of sporadic Yersinia enterocolitica bioserotype 4/O:3 strains from human and porcine sources. Epidemiol Infect 127: 37–47. PubMed PMC

Fredriksson-Ahomaa M, Korkeala H (2003) Low occurrence of pathogenic Yersinia enterocolitica in clinical, food, and environmental samples: a methodological problem. Clin Microbiol Rev 16: 220–229. PubMed PMC

Wang X, Cui Z, Jin D, Tang L, Xia S, et al. (2009) Distribution of pathogenic Yersinia enterocolitica in China. Eur J Clin Microbiol Infect Dis 28: 1237–1244. PubMed

European Food Safety Authority (2012) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2010. EFSA J 10: e2597 10.2903/j.efsa.2012.2597 PubMed DOI PMC

Marriott DJ, Taylor S, Dorman DC (1985) Yersinia enterocolitica infection in children. Med J Aust 143: 489–492. PubMed

Lee LA, Gerber AR, Lonsway DR, Smith JD, Carter GP, et al. (1990) Yersinia enterocolitica O:3 infections in infants and children, associated with the household preparation of chitterlings. N Engl J Med 322: 984–987. PubMed

Lee LA, Taylor J, Carter GP, Quinn B, Farmer JJ, et al. (1991) Yersinia enterocolitica O:3: an emerging cause of pediatric gastroenteritis in the United States. J Infect Dis 163: 660–663. PubMed

Gray JT, WaKabongo M, Campos FE, Diallo AA, Tyndal C, et al. (2001) Recognition of Yersinia enterocolitica multiple strain infection in twin infants using PCR-based DNA fingerprinting. J Appl Microbiol 90: 358–364. PubMed

Ray SM, Ahuja SD, Blake PA, Farley MM, Samuel M, et al. (2004) Population-based surveillance for Yersinia enterocolitica infections in FoodNet Sites, 1996–1999: Higher risk of disease in infants and minority populations. Clin Infect Dis 38(s3): S181–S189 10.1086/381585 PubMed DOI

Pai CH, Gillis F, Tuomanen E, Marks MI (1984) Placebo-controlled double-blind evaluation of trimethoprim-sulfamethoxazole treatment of Yersinia enterocolitica gastroenteritis. J Pediatr 104: 308–311. PubMed

Hoogkamp-Korstanje JA, Stolk-Engelaar VM (1995) Yersinia enterocolitica infection in children. Pediatr Infect Dis J 14: 771–775. PubMed

Abdel-Haq NM, Asmar BI, Abuhammour WM, Brown WJ (2000) Yersinia enterocolitica infection in children. Pediatr Infect Dis J 19: 954–958. PubMed

Cascales E, Buchanan SK, Duché D, Kleanthous C, Lloubès R, et al. (2007) Colicin biology. Microbiol Mol Biol Rev 71: 158–229. PubMed PMC

Ben-Gurion R, Hertman I (1958) Bacteriocin-like material produced by Pasteurella pestis . J Gen Microbiol 19: 289–297. PubMed

Bottone EJ, Sandhu KK, Pisano MA (1979) Yersinia intermedia: temperature-dependent bacteriocin production. J Clin Microbiol 10: 433–436. PubMed PMC

Calvo C, Brault J, Ramos-Cormenzana A, Mollaret HH (1986) Production of bacteriocin-like substances by Yersinia frederiksenii, Y. kristensenii, and Y. intermedia strains. Folia Microbiol 31: 177–186. PubMed

Cafferkey MT, McClean K, Drumm ME (1989) Production of bacteriocin-like antagonism by clinical isolates of Yersinia enterocolitica . J Clin Microbiol 27: 677–680. PubMed PMC

Csiszár K, Tóth I (1992) Bacteriocin-like antagonism in Yersinia enterocolitica . Acta Microbiol Hung 39: 193–201. PubMed

Toora S, Budu-Amoako E, Ablett RF, Smith J (1994) Inhibition and inactivation of pathogenic serogroups of Yersinia enterocolitica by a bacteriocin produced by Yersinia kristensenii . Lett App Microbiol 19: 40–43.

Ferber DM, Brubaker RR (1979) Mode of action of pesticin: N-acetylglucosaminidase activity. J Bacteriol 139: 495–501. PubMed PMC

Rakin A, Saken E, Harmsen D, Heesemann J (1994) The pesticin receptor of Yersinia enterocolitica: a novel virulence factor with dual function. Mol Microbiol 13: 253–263. PubMed

Pilsl H, Killmann H, Hantke K, Braun V (1996) Periplasmic location of the pesticin immunity protein suggests inactivation of pesticin in the periplasm. J Bacteriol 178: 2431–2435. PubMed PMC

Rakin A, Boolgakowa E, Heesemann J (1996) Structural and functional organization of the Yersinia pestis bacteriocin pesticin gene cluster. Microbiology 142: 3415–3424. PubMed

Vollmer W, Pilsl H, Hantke K, Höltje JV, Braun V (1997) Pesticin displays muramidase activity. J Bacteriol 179: 1580–1583. PubMed PMC

Patzer SI, Albrecht R, Braun V, Zeth K (2012) Structural and mechanistic studies of pesticin, a bacterial homolog of phage lysozymes. J Biol Chem 287: 23381–23396. PubMed PMC

Strauch E, Kaspar H, Schaudinn C, Dersch P, Madela K, et al. (2001) Characterization of enterocoliticin, a phage tail-like bacteriocin, and its effect on pathogenic Yersinia enterocolitica strains. Appl Environ Microbiol 67: 5634–5642. PubMed PMC

Damasko C, Konietzny A, Kaspar H, Appel B, Dersch P, et al. (2005) Studies of the efficacy of enterocoliticin, a phage-tail like bacteriocin, as antimicrobial agent against Yersinia enterocolitica serotype O3 in a cell culture system and in mice. J Vet Med B 52: 171–179. PubMed

Bosák J, Laiblová P, Šmarda J, Dedicová D, Šmajs D (2012) Novel colicin FY of Yersinia frederiksenii inhibits pathogenic Yersinia strains via YiuR-mediated reception, TonB import, and cell membrane pore formation. J Bacteriol 194: 1950–1959. PubMed PMC

Kotetishvili M, Kreger A, Wauters G, Morris JG, Sulakvelidze A, et al. (2005) Multilocus sequence typing for studying genetic relationships among Yersinia species. J Clin Microbiol 43: 2674–2684. PubMed PMC

Neubauer H, Aleksic S, Hensel A, Finke EJ, Meyer H (2000) Yersinia enterocolitica 16S rRNA gene types belong to the same genospecies but form three homology groups. Int J Med Microbiol 290: 61–64. PubMed

Harnett N, Lin YP, Krishnan C (1996) Detection of pathogenic Yersinia enterocolitica using the multiplex polymerase chain reaction. Epidemiol Infect 117: 59–67. PubMed PMC

Clinical and Laboratory Standards Institute (2012) Performance standards for antimicrobial disk susceptibility tests; Approved standard - Eleventh edition. Clinical and Laboratory Standards Institute.Wayne PA. 58.

Šmarda J, Šmajs D, Horynová S (2006) Incidence of lysogenic, colicinogenic and siderophore-producing strains among human non-pathogenic Escherichia coli . Folia Microbiol 51: 387–391. PubMed

Bissett ML, Powers C, Abbott SL, Janda JM (1990) Epidemiologic investigations of Yersinia enterocolitica and related species: sources, frequency, and serogroup distribution. J Clin Microbiol 28: 910–902. PubMed PMC

Batzilla J, Antonenka U, Höper D, Heesemann J, Rakin A (2011) Yersinia enterocolitica palearctica serobiotype O:3/4 - a successful group of emerging zoonotic pathogens. BMC Genomics 12: e348 10.1186/1471-2164-12-348 PubMed DOI PMC

Rahman A, Bonny TS, Stonsaovapak S, Ananchaipattana C (2011) Yersinia enterocolitica: Epidemiological studies and outbreaks. J Pathog 2011: e239391 10.4061/2011/239391 PubMed DOI PMC

Saken E, Roggenkamp A, Aleksic S, Heesemann J (1994) Characterisation of pathogenic Yersinia enterocolitica serogroups by pulsed-field gel electrophoresis of genomic NotI restriction fragments. J Med Microbiol 41: 329–338. PubMed

Najdenski H, Iteman I, Carniel E (1994) Efficient subtyping of pathogenic Yersinia enterocolitica strains by pulsed-field gel electrophoresis. J Clin Microbiol 32: 2913–2920. PubMed PMC

Iteman I, Guiyoule A, Carniel E (1996) Comparison of three molecular methods for typing and subtyping pathogenic Yersinia enterocolitica strains. J Med Microbiol 45: 48–56. PubMed

Asplund K, Johansson T, Siitonen A (1998) Evaluation of pulsed-field gel electrophoresis of genomic restriction fragments in the discrimination of Yersinia enterocolitica O:3. Epidemiol Infect 121: 579–586. PubMed PMC

Zheng H, Sun Y, Mao Z, Jiang B (2008) Investigation of virulence genes in clinical isolates of Yersinia enterocolitica . FEMS Immunol Med Microbiol 53: 368–374. PubMed

Fàbrega A, Vila J (2012) Yersinia enterocolitica: pathogenesis, virulence and antimicrobial resistance. Enferm Infecc Microbiol Clin 30: 24–32. PubMed

Stock I, Wiedemann B (1999) An in-vitro study of the antimicrobial susceptibilities of Yersinia enterocolitica and the definition of a database. J Antimicrob Chemother 43: 37–45. PubMed

Riley MA, Gordon DM (1999) The ecological role of bacteriocins in bacterial competition. Trends Microbiol 7: 129–133. PubMed

Kerr B, Riley MA, Feldman MW, Bohannan BJM (2002) Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors. Nature 418: 171–174. PubMed

Nahum JR, Harding BN, Kerr B (2011) Evolution of restraint in a structured rock–paper–scissors community. Proc Natl Acad Sci U S A 108 (s2): 10831–10838 10.1073/pnas.1100296108 PubMed DOI PMC

Feldgarden M, Riley MA (1998) High levels of colicin resistance in Escherichia coli . Evolution 52: 1270–1276. PubMed

Gordon DM, Riley MA, Pinou T (1998) Temporal changes in the frequency of colicinogeny in Escherichia coli from house mice. Microbiology 144: 2233–2240. PubMed

Toora S (1995) Partial purification and characterization of bacteriocin from Yersinia kristensenii . J Appl Bacteriol 78: 224–228. PubMed

Toora S (1995) Application of Yersinia kristensenii bacteriocin as a specific marker for the rapid identification of suspected isolates of Yersinia enterocolitica . Lett Appl Microbiol 20: 171–174. PubMed

Bhaduri S, Wesley I, Richards H, Draughon A, Wallace M (2009) Clonality and antibiotic susceptibility of Yersinia enterocolitica isolated from U.S. market weight hogs. Foodborne Pathog Dis 6: 351–356. PubMed

Sihvonen LM, Jalkanen K, Huovinen E, Toivonen S, Corander J, et al. (2012) Clinical isolates of Yersinia enterocolitica Biotype 1A represent two phylogenetic lineages with differing pathogenicity-related properties. BMC Microbiology 12: 208 10.1186/1471-2180-12-208 PubMed DOI PMC

Kirillina O, Bobrov AG, Fetherston JD, Perry RD (2006) Hierarchy of iron uptake systems: Yfu and Yiu are functional in Yersinia pestis . Infect Immun 74: 6171–6178. PubMed PMC

Chen PE, Cook C, Stewart AC, Nagarajan N, Sommer DD, et al. (2010) Genomic characterization of the Yersinia genus. Genome Biol 11: R1 10.1186/gb-2010-11-1-r1 PubMed DOI PMC

Reuter S, Thomson NR, McNally A (2012) Evolutionary dynamics of the Yersinia enterocolitica complex. Adv Exp Med Biol 954: 15–22 10.1007/978-1-4614-3561-72 PubMed DOI

Shayegani M, DeForge I, McGlynn DM, Root T (1981) Characteristics of Yersinia enterocolitica and related species isolated from human, animal, and environmental sources. J Clin Microbiol 14: 304–312. PubMed PMC

Greenwood M, Hooper WL (1987) Human carriage of Yersinia spp. J Med Microbiol 23: 345–348. PubMed

Soltan-Dallal MM, Moezardalan K (2004) Frequency of Yersinia species infection in paediatric acute diarrhoea in Tehran. East Mediterr Health J 10: 152–158. PubMed

Lodinová-Zádniková R, Sonnenborn U (1997) Effect of preventive administration of a nonpathogenic Escherichia coli strain on the colonization of the intestine with microbial pathogens in newborn infants. Biol Neonate 71: 224–232. PubMed

Patzer SI, Baquero MR, Bravo D, Moreno F, Hantke K (2003) The colicin G, H and X determinants encode microcins M and H47, which might utilize the catecholate siderophore receptors FepA, Cir, Fiu and IroN. Microbiology 149: 2557–2570. PubMed

Cursino L, Šmajs D, Šmarda J, Nardi RM, Nicoli JR, et al. (2006) Exoproducts of the Escherichia coli strain H22 inhibiting some enteric pathogens both in vitro and in vivo . J Appl Microbiol 100: 821–829. PubMed

Wooley RE, Gibbs PS, Shotts EB Jr (1999) Inhibition of Salmonella typhimurium in the chicken intestinal tract by a transformed avirulent avian Escherichia coli . Avian Dis 43: 245–250. PubMed

Escherichia coli Strains Producing Selected Bacteriocins Inhibit Porcine Enterotoxigenic Escherichia coli (ETEC) under both In Vitro and In Vivo Conditions

Colicin Z, a structurally and functionally novel colicin type that selectively kills enteroinvasive Escherichia coli and Shigella strains

Colicin FY inhibits pathogenic Yersinia enterocolitica in mice