Analysis of iron acquisition and storage-related genes in clinical and non-clinical strains of Yersinia enterocolitica biovar 1A
Pawan Kumar Kanaujia
Microbial Pathogenicity Laboratory, Department of Microbiology, University of Delhi South Campus, New Delhi, India
Search for more papers by this authorPriyanka Bajaj
Microbial Pathogenicity Laboratory, Department of Microbiology, University of Delhi South Campus, New Delhi, India
Search for more papers by this authorCorresponding Author
Jugsharan Singh Virdi
Microbial Pathogenicity Laboratory, Department of Microbiology, University of Delhi South Campus, New Delhi, India
Jugsharan Singh Virdi, Microbial Pathogenicity Laboratory, Department of Microbiology, University of Delhi South Campus, Benito Juarez Road, New Delhi, 110021, India. e-mail: [email protected]Search for more papers by this authorPawan Kumar Kanaujia
Microbial Pathogenicity Laboratory, Department of Microbiology, University of Delhi South Campus, New Delhi, India
Search for more papers by this authorPriyanka Bajaj
Microbial Pathogenicity Laboratory, Department of Microbiology, University of Delhi South Campus, New Delhi, India
Search for more papers by this authorCorresponding Author
Jugsharan Singh Virdi
Microbial Pathogenicity Laboratory, Department of Microbiology, University of Delhi South Campus, New Delhi, India
Jugsharan Singh Virdi, Microbial Pathogenicity Laboratory, Department of Microbiology, University of Delhi South Campus, Benito Juarez Road, New Delhi, 110021, India. e-mail: [email protected]Search for more papers by this authorAbstract
Possession of mechanisms for iron acquisition and its storage enhances the ability of the bacteria to survive in the iron-limiting environment of the host. In this study, 81 strains of Yersinia enterocolitica biovar 1A isolated from various clinical (n = 51) and non-clinical (n = 30) sources were investigated for the presence of the genes related to iron acquisition and storage. Important genes which were present in more than 85% of the strains included hasA, foxA, bfr, bfd, ftnA, and hmsT as well as the fhuCDB, fepBDGCfesfepA, feoAB, yfuABCD, hemPRSTUV, and hmsHFRS gene clusters. Majority of these genes is being reported for the first time in biovar 1A strains and showed significant homology with genes present in the known pathogenic biovars of Y. enterocolitica. However, no significant difference was observed in the distribution of iron acquisition and storage-related genes among clinical and non-clinical biovar 1A strains. Thus, it may be suggested that the presence of iron acquisition and storage-related genes per se might not be responsible for the supposedly better ability of clinical biovar 1A strains to cause infections in humans. However, in the backdrop of this data, the need to undertake functional studies are highly recommended.
References
- 1Bottone EJ. Yersinia enterocolitica: the charisma continues. Clin Microbiol Rev 1997; 10: 257–76.
- 2Bottone EJ. Yersinia enterocolitica: overview and epidemiologic correlates. Microbes Infect 1999; 1: 323–33.
- 3Cornelis GR, Boland A, Boyd AP, Geuijen C, Iriarte M, Neyt C, et al. The virulence plasmid of Yersinia, an antihost genome. Microbiol Mol Biol Rev 1998; 62: 1315–52.
- 4Revell PA, Miller VL. Yersinia virulence: more than a plasmid. FEMS Microbiol Lett 2001; 205: 159–64.
- 5Robins-Browne RM, Miliotis MD, Cianciosi S, Miller VL, Falkow S, Morris JG Jr. Valuation of DNA colony hybridization and other techniques for detection of virulence in Yersinia species. J Clin Microbiol 1989; 27: 644–50.
- 6Morris JG Jr, Prado V, Ferreccio C, Robins-Browne RM, Bordun AM, Cayazzo M, et al. Yersinia enterocolitica isolated from two cohorts of young children in Santiago, Chile: incidence of lack of correlation between illness and proposed virulence factors. J Clin Microbiol 1991; 29: 2784–8.
- 7Burnens AP, Frey A, Nicolet J. Association between clinical presentation, biogroups and virulence attributes of Yersinia enterocolitica strains in human diarrhoeal disease. Epidemiol Infect 1996; 116: 27–34.
- 8Ratnam S, Mercer E, Picco B, Parsons S, Butler R. A nosocomial outbreak of diarrheal disease due to Yersinia enterocolitica serotype O:5, biotype 1. J Infect Dis 1982; 145: 242–7.
- 9Greenwood MH, Hooper WL. Excretion of Yersinia spp. associated with consumption of pasteurized milk. Epidemiol Infect 1990; 104: 345–50.
- 10Sachdeva P, Virdi JS. Repetitive elements sequence (REP/ERIC)-PCR based genotyping of clinical and environmental strains of Yersinia enterocolitica biotype 1A reveal existence of limited number of clonal groups. FEMS Microbiol Lett 2004; 240: 193–201.
- 11Gulati P, Varshney RK, Virdi JS. Multilocus variable number tandem repeat analysis as a tool to discern genetic relationships among strains of Yersinia enterocolitica biovar 1A. J Appl Microbiol 2009; 107: 875–84.
- 12Mallik S, Virdi JS. Genetic relationships between clinical and non-clinical strains of Yersinia enterocolitica biovar 1A as revealed by multilocus enzyme electrophoresis and multilocus restriction typing. BMC Microbiol 2010; 10: 158.
- 13Sihvonen LM, Jalkanen K, Huovinen E, Toivonen S, Corander J, Kuusi M, et al. Clinical isolates of Yersinia enterocolitica biotype 1A represent two phylogenetic lineages with differing pathogenicity-related properties. BMC Microbiol 2012; 12: 208.
- 14Campioni F, Falcão JP. Genotypic diversity and virulence markers of Yersinia enterocolitica biotype 1A strains isolated from clinical and non-clinical origins. APMIS 2014; 122: 215–22.
- 15Robins-Browne RM, Tzipori S, Gonis G, Hayes J, Withers M, Prpic JK. The pathogenesis of Yersinia enterocolitica infection in gnotobiotic piglets. J Med Microbiol 1985; 19: 297–308.
- 16Tennant SM, Grant TH, Robins-Browne RM. Pathogenicity of Yersinia enterocolitica biotype 1A. FEMS Immunol Med Microbiol 2003; 38: 127–37.
- 17Chambers CE, Sokol PA. Comparison of siderophore production and utilization in pathogenic and environmental isolates of Yersinia enterocolitica. J Clin Microbiol 1994; 32: 32–9.
- 18Tennant SM, Skinner NA, Joe A, Robins-Browne RM. Homologues of insecticidal toxin complex genes in Yersinia enterocolitica biotype 1A and their contribution to virulence. Infect Immun 2005; 73: 6860–7.
- 19Bach S, De Almeida A, Carniel E. The Yersinia high-pathogenicity island is present in different members of the family Enterobacteriaceae. FEMS Microbiol Lett 2000; 183: 289–94.
- 20Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011; 28: 2731–9.
- 21Carniel E. The Yersinia high-pathogenicity island: an iron-uptake island. Microbes Infect 2001; 3: 561–9.
- 22Miller DA, Luo L, Hillson N, Keating TA, Walsh CT. Yersiniabactin synthetase: a four-protein assembly line producing the nonribosomal peptide/polyketide hybrid siderophore of Yersinia pestis. Chem Biol 2002; 9: 333–44.
- 23Schubert S, Fischer D, Heesemann J. Ferric enterochelin transport in Yersinia enterocolitica: molecular and evolutionary aspects. J Bacteriol 1999; 181: 6387–95.
- 24Batzilla J, Heesemann J, Rakin A. The pathogenic potential of Yersinia enterocolitica 1A. Int J Med Microbiol 2011; 301: 556–61.
- 25Báumler AJ, Hantke K. Ferrioxamine uptake in Yersinia enterocolitica: characterization of the receptor protein FoxA. Mol Microbiol 1992; 6: 1309–21.
- 26Koebnik R, Hantke K, Braun V. The TonB-dependent ferrichrome receptor FcuA of Yersinia enterocolitica: evidence against a strict co-evolution of receptor structure and substrate specificity. Mol Microbiol 1993; 7: 383–93.
- 27Batzilla J, Höper D, Antonenka U, Heesemann J, Rakin A. Complete genome sequence of Yersinia enterocolitica subsp. palearctica serogroup O:3. J Bacteriol 2011; 193: 2067.
- 28Wang X, Li Y, Jing H, Ren Y, Zhou Z, Wang S, et al. Complete genome sequence of a Yersinia enterocolitica “Old World” (3/O:9) strain and comparison with the “New World” (1B/O:8) strain. J Clin Microbiol 2011; 49: 1251–9.
- 29Mademidis A, Köster W. Transport activity of FhuA, FhuC, FhuD, and FhuB derivatives in a system free of polar effects, and stoichiometry of components involved in ferrichrome uptake. Mol Gen Genet 1998; 258: 156–65.
- 30Ratledge C, Dover LG. Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 2000; 54: 881–941.
- 31Stojiljkovic I, Hantke K. Transport of haemin across the cytoplasmic membrane through a haemin-specific periplasmic binding-protein-dependent transport system in Yersinia enterocolitica. Mol Microbiol 1994; 13: 719–32.
- 32Rossi MS, Fetherston JD, Létoffé S, Carniel E. Identification and characterization of the hemophore-dependent heme acquisition system of Yersinia pestis. Infect Immun 2001; 69: 6707–17.
- 33Saken E, Rakin A, Heesemann J. Molecular characterization of a novel siderophore-independent iron transport system in Yersinia. Int J Med Microbiol 2000; 290: 51–60.
- 34Garg RP, Vargo CJ, Cui X, Kurtz DM Jr. A [2Fe-2S] protein encoded by an open reading frame upstream of the Escherichia coli bacterioferritin gene. Biochemistry 1996; 35: 6297–301.
- 35Quail MA, Jordan P, Grogan JM, Butt JN, Lutz M, Thomson AJ, et al. Spectroscopic and voltammetric characterisation of the bacterioferritin- associated ferredoxin of Escherichia coli. Biochem Biophys Res commun 1996; 229: 635–42.
- 36Hinnebusch BJ, Erickson DL. Yersinia pestis biofilm in the flea vector and its role in the transmission of plague. Curr Top Microbiol Immunol 2008; 322: 229–48.
- 37Perry RD, Bobrov AG, Kirillina O, Jones HA, Pedersen L, Abney J, et al. Temperature regulation of the hemin storage (Hms +) phenotype of Yersinia pestis is posttranscriptional. J Bacteriol 2004; 186: 1638–47.
- 38Lillard JW Jr, Bearden SW, Fetherston JD, Perry RD. The haemin storage (Hms +) phenotype of Yersinia pestis is not essential for the pathogenesis of bubonic plague in mammals. Microbiology 1999; 145: 197–209.
- 39Kanaujia PK, Bajaj P, Kumar S, Singhal N, Virdi JS. Proteomic analysis of Yersinia enterocolitica biovar 1A under iron-rich and iron-poor conditions indicate existence of efficiently regulated mechanisms of iron homeostasis. J Proteomics 2015; 124: 39–49.