Characterization of temperate phages infecting Clostridium difficile isolates of human and animal origins

Applied and Environmental Microbiology

Volumn 80, Issue 8, 2014, Pages 2555-2563

  Sekulovic, Ognjen ^a   Garneau, Julian R ^a   Néron, Audrey ^a   Fortier, Louis Charles ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CLOSTRIDIUM; ELECTROPHORESIS;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC RESISTANCE GENES; CLOSTRIDIUM DIFFICILE; DOUBLE STRANDED DNA; GRAM-POSITIVE PATHOGENS; POTENTIAL RESERVOIR; PULSED FIELD GEL ELECTROPHORESIS; RESTRICTION ENZYMES;

BACTERIOPHAGES;

DISEASE INCIDENCE; DISEASE TRANSMISSION; ENZYME ACTIVITY; GENE EXPRESSION; HEALTH RISK; INFECTIOUS DISEASE; INFECTIVITY; MICROBIAL ACTIVITY; PATHOGEN;

VIRUS DNA;

ANIMAL; BACTERIOPHAGE; CHEMISTRY; CLOSTRIDIUM INFECTION; DNA FINGERPRINTING; DOG; GENETICS; GROWTH, DEVELOPMENT AND AGING; HORSE; HOST RANGE; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR WEIGHT; MYOVIRIDAE; PEPTOCLOSTRIDIUM DIFFICILE; PHYSIOLOGY; PROPHAGE; PULSED FIELD GEL ELECTROPHORESIS; RESTRICTION MAPPING; SIPHOVIRIDAE; ULTRASTRUCTURE; VETERINARY; VIROLOGY;

ANIMALS; BACTERIOPHAGES; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM INFECTIONS; DNA FINGERPRINTING; DNA, VIRAL; DOGS; ELECTROPHORESIS, GEL, PULSED-FIELD; HORSES; HOST SPECIFICITY; HUMANS; MOLECULAR WEIGHT; MYOVIRIDAE; PROPHAGES; RESTRICTION MAPPING; SIPHOVIRIDAE;

EID: 84896992962     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00237-14     Document Type: Article

References (59)

1. He M, Miyajima F, Roberts P, Ellison L, Pickard DJ, Martin MJ, Connor TR, Harris SR, Fairley D, Bamford KB, D'Arc S, Brazier J, Brown D, Coia JE, Douce G, Gerding D, Kim HJ, Koh TH, Kato H, Senoh M, Louie T, Michell S, Butt E, Peacock SJ, Brown NM, Riley T, Songer G, Wilcox M, Pirmohamed M, Kuijper E, Hawkey P, Wren BW, Dougan G, Parkhill J, Lawley TD. 2013. Emergence and global spread of epidemic healthcare-associated Clostridium difficile. Nat. Genet. 45:109-113. http://dx.doi.org/10.1038/ng.2478.
2. Arroyo LG, Kruth SA, Willey BM, Staempfli HR, Low DE, Weese JS. 2005. PCR ribotyping of Clostridium difficile isolates originating from human and animal sources. J. Med. Microbiol. 54:163-166. http://dx.doi.org/10.1099/jmm.0.45805-0.
3. Rupnik M, Wilcox MH, Gerding DN. 2009. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat. Rev. Microbiol. 7:526-536. http://dx.doi.org/10.1038/nrmicro2164.
4. Loo V, Poirier L, Miller M, Oughton M, Libman M, Michaud S, Bourgault A, Nguyen T, Frenette C, Kelly M, Vibien A, Brassard P, Fenn S, Dewar K, Hudson T, Horn R, Rene P, Monczak Y, Dascal A. 2005. A predominantly clonal multi-institutional outbreak of Clostridium difficile-associated diarrhea with high morbidity and mortality. N. Engl. J. Med. 353:2442-2449. http://dx.doi.org/10.1056/NEJMoa051639.
5. Barbut F, Jones G, Eckert C. 2011. Epidemiology and control of Clostridium difficile infections in healthcare settings: an update. Curr. Opin. Infect. Dis. 24:370-376. http://dx.doi.org/10.1097/QCO.0b013e3283474 8e5.
6. Cheknis AK, Sambol SP, Davidson DM, Nagaro KJ, Mancini MC, Hidalgo-Arroyo GA, Brazier JS, Johnson S, Gerding DN. 2009. Distribution of Clostridium difficile strains from a North American, European and Australian trial of treatment for C. difficile infections: 2005-2007. Anaerobe 15:230-233. http://dx.doi.org/10.1016/j.anaerobe.2009.09.001.
7. Centers for Disease Control and Prevention. 2005. Severe Clostridium difficile-associated disease in populations previously at low risk-four states, 2005. MMWR Morb. Mortal. Wkly. Rep. 54:1201-1205.
8. Rupnik M, Widmer A, Zimmermann O, Eckert C, Barbut F. 2008. Clostridium difficile toxinotype V, ribotype 078, in animals and humans. J. Clin. Microbiol. 46:2146. (Letter.) http://dx.doi.org/10.1128/JCM.00598-08.
9. Rupnik M. 2007. Is Clostridium difficile-associated infection a potentially zoonotic and foodborne disease? Clin. Microbiol. Infect. 13:457-459. http://dx.doi.org/10.1111/j.1469-0691.2007.01687.x.
10. Weese JS, Finley R, Reid-Smith RR, Janecko N, Rousseau J. 2010. Evaluation of Clostridium difficile in dogs and the household environment. Epidemiol. Infect. 138:1100-1104. http://dx.doi.org/10.1017/S09502688 09991312.
11. Canchaya C, Fournous G, Brüssow H. 2004. The impact of prophages on bacterial chromosomes. Mol. Microbiol. 53:9-18. http://dx.doi.org/10.1111/j.1365-2958.2004.04113.x.
12. Bidet P, Barbut F, Lalande V, Burghoffer B, Petit JC. 1999. Development of a new PCR-ribotyping method for Clostridium difficile based on ribosomal RNA gene sequencing. FEMS Microbiol. Lett. 175:261-266. http://dx.doi.org/10.1111/j.1574-6968.1999.tb13629.x.
13. van den Berg R, Schaap I, Templeton K, Klaassen C, Kuijper E. 2007. Typing and subtyping of Clostridium difficile isolates by using multiplelocus variable-number tandem-repeat analysis. J. Clin. Microbiol. 45: 1024-1028. http://dx.doi.org/10.1128/JCM.02023-06.
14. Lemee L, Dhalluin A, Pestel-Caron M, Lemeland J-F, Pons J-L. 2004. Multilocus sequence typing analysis of human and animal Clostridium difficile isolates of various toxigenic types. J. Clin. Microbiol. 42:2609-2617. http://dx.doi.org/10.1128/JCM.42.6.2609-2617.2004.
15. Sebaihia M, Wren BW, Mullany P, Fairweather NF, Minton N, Stabler R, Thomson NR, Roberts AP, Cerdeño-Tárraga AM, Wang H, Holden MTG, Wright A, Churcher C, Quail MA, Baker S, Bason N, Brooks K, Chillingworth T, Cronin A, Davis P, Dowd L, Fraser A, Feltwell T, Hance Z, Holroyd S, Jagels K, Moule S, Mungall K, Price C, Rabbinowitsch E, Sharp S, Simmonds M, Stevens K, Unwin L, Whithead S, Dupuy B, Dougan G, Barrell B, Parkhill J. 2006. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat. Genet. 38:779-786. http://dx.doi.org/10.1038/ng1830.
16. Hubert B, Loo VG, Bourgault A-M, Poirier L, Dascal A, Fortin E, Dionne M, Lorange M. 2007. A portrait of the geographic dissemination of the Clostridium difficile North American pulsed-field type 1 strain and the epidemiology of C. difficile-associated disease in Québec. Clin. Infect. Dis. 44:238-244. http://dx.doi.org/10.1086/510391.
17. Fortier L-C, Moineau S. 2007. Morphological and genetic diversity of temperate phages in Clostridium difficile. Appl. Environ. Microbiol. 73: 7358-7366. http://dx.doi.org/10.1128/AEM.00582-07.
18. Nale JY, Shan J, Hickenbotham PT, Fawley WN, Wilcox MH, Clokie MRJ. 2012. Diverse temperate bacteriophage carriage in Clostridium difficile 027 strains. PLoS One 7:e37263. http://dx.doi.org/10.1371/journal.pone.0037263.
19. Shan J, Patel KV, Hickenbotham PT, Nale JY, Hargreaves KR, Clokie MRJ. 2012. Prophage carriage and diversity within clinically relevant strains of Clostridium difficile. Appl. Environ. Microbiol. 78:6027-6034. http://dx.doi.org/10.1128/AEM.01311-12.
20. Hargreaves KR, Colvin HV, Patel KV, Clokie JJP, Clokie MRJ. 2013. Genetically diverse Clostridium difficile strains harboring abundant prophages in an estuarine environment. Appl. Environ. Microbiol. 79:6236-6243. http://dx.doi.org/10.1128/AEM.01849-13.
21. Goh S, Riley TV, Chang BJ. 2005. Isolation and characterization of temperate bacteriophages of Clostridium difficile. Appl. Environ. Microbiol. 71: 1079-1083. http://dx.doi.org/10.1128/AEM.71.2.1079-1083.2005.
22. Gebhart D, Williams SR, Bishop-Lilly KA, Govoni GR, Willner KM, Butani A, Sozhamannan S, Martin D, Fortier L-C, Scholl D. 2012. Novel high-molecular-weight, R-type bacteriocins of Clostridium difficile. J. Bacteriol. 194:6240-6247. http://dx.doi.org/10.1128/JB.01272-12.
23. Ackermann H-W. 2009. Phage classification and characterization. Methods Mol. Biol. 501:127-140. http://dx.doi.org/10.1007/978-1-60327-164-6_13.
24. Govind R, Fralick J, Rolfe R. 2006. Genomic organization and molecular characterization of Clostridium difficile bacteriophage {Phi}CD119. J. Bacteriol. 188:2568-2577. http://dx.doi.org/10.1128/JB.188.7.2568-2577.2006.
25. Goh S, Ong PF, Song KP, Riley TV, Chang BJ. 2007. The complete genome sequence of Clostridium difficile phage phiC2 and comparisons to phiCD119 and inducible prophages of CD630. Microbiology 153:676-685. http://dx.doi.org/10.1099/mic.0.2006/002436-0.
26. Mayer MJ, Narbad A, Gasson MJ. 2008. Molecular characterization of a Clostridium difficile bacteriophage and its cloned biologically active endolysin. J. Bacteriol. 190:6734-6740. http://dx.doi.org/10.1128/JB.00686-08.
27. Meessen-Pinard M, Sekulovic O, Fortier L-C. 2012. Evidence of in vivo prophage induction during Clostridium difficile infection. Appl. Environ. Microbiol. 78:7662-7670. http://dx.doi.org/10.1128/AEM.02275-12.
28. Sekulovic O, Meessen-Pinard M, Fortier L-C. 2011. Prophagestimulated toxin production in Clostridium difficile NAP1/027 lysogens. J. Bacteriol. 193:2726-2734. http://dx.doi.org/10.1128/JB.00787-10.
29. Horgan M, O'Sullivan O, Coffey A, Fitzgerald GF, van Sinderen D, McAuliffe O, Ross RP. 2010. Genome analysis of the Clostridium difficile phage PhiCD6356, a temperate phage of the Siphoviridae family. Gene 462:34-43. http://dx.doi.org/10.1016/j.gene.2010.04.010.
30. Brüssow H, Canchaya C, Hardt W-D. 2004. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68:560-602. http://dx.doi.org/10.1128/MMBR.68.3.560-602.2004.
31. Fortier L-C, Sekulovic O. 2013. Importance of prophages to evolution and virulence of bacterial pathogens. Virulence 4:354-365. http://dx.doi.org/10.4161/viru.24498.
32. Govind R, Vediyappan G, Rolfe RD, Dupuy B, Fralick JA. 2009. Bacteriophage-mediated toxin gene regulation in Clostridium difficile. J. Virol. 83:12037-12045. http://dx.doi.org/10.1128/JVI.01256-09.
33. Sirard S, Valiquette L, Fortier L-C. 2011. Lack of association between clinical outcome of Clostridium difficile infections, strain type, and virulence-associated phenotypes. J. Clin. Microbiol. 49:4040-4046. http://dx.doi.org/10.1128/JCM.05053-11.
34. Fortier L-C, Moineau S. 2009. Phage production and maintenance of stocks, including expected stock lifetimes. Methods Mol. Biol. 501:203-219. http://dx.doi.org/10.1007/978-1-60327-164-6_19.
35. Moineau S, Pandian S, Klaenhammer T. 1994. Evolution of a lytic bacteriophage via DNA acquisition from the Lactococcus lactis chromosome. Appl. Environ. Microbiol. 60:1832-1841.
36. Freeman J, Bauer MP, Baines SD, Corver J, Fawley WN, Goorhuis B, Kuijper EJ, Wilcox MH. 2010. The changing epidemiology of Clostridium difficile infections. Clin. Microbiol. Rev. 23:529-549. http://dx.doi.org/10.1128/CMR.00082-09.
37. Didelot X, Eyre D, Cule M, Ip C, Ansari A, Griffiths D, Vaughan A, O'Connor L, Golubchik T, Batty E, Piazza P, Wilson D, Bowden R, Donnelly P, Dingle K, Wilcox M, Walker S, Crook D, Peto T, Harding R. 2012. Microevolutionary analysis of Clostridium difficile genomes to investigate transmission. Genome Biol. 13:R118. http://dx.doi.org/10.1186/gb-2012-13-12-r118.
38. Stabler RA, Gerding DN, Songer JG, Drudy D, Brazier JS, Trinh HT, Witney AA, Hinds J, Wren BW. 2006. Comparative phylogenomics of Clostridium difficile reveals clade specificity and microevolution of hypervirulent strains. J. Bacteriol. 188:7297-7305. http://dx.doi.org/10.1128/JB.00664-06.
39. Stabler RA, He M, Dawson L, Martin M, Valiente E, Corton C, Lawley TD, Sebaihia M, Quail MA, Rose G, Gerding DN, Gibert M, Popoff MR, Parkhill J, Dougan G, Wren BW. 2009. Comparative genome and phenotypic analysis of Clostridium difficile 027 strains provides insight into the evolution of a hypervirulent bacterium. Genome Biol. 10:R102. http://dx.doi.org/10.1186/gb-2009-10-9-r102.
40. Walk ST, Micic D, Jain R, Lo ES, Trivedi I, Liu EW, Almassalha LM, Ewing SA, Ring C, Galecki AT, Rogers MAM, Washer L, Newton DW, Malani PN, Young VB, Aronoff DM. 2012. Clostridium difficile ribotype does not predict severe infection. Clin. Infect. Dis. 55:1661-1668. http://dx.doi.org/10.1093/cid/cis786.
41. Barbut F, Rupnik M. 2012. Editorial commentary: 027, 078, and others: going beyond the numbers (and away from the hypervirulence). Clin. Infect. Dis. 55:1669-1672. http://dx.doi.org/10.1093/cid/cis790.
42. Bauer MP, Notermans DW, Van Benthem BH, Brazier JS, Wilcox MH, Rupnik M, Monnet DL, van Dissel JT, Kuijper EJ. 2011. Clostridium difficile infection in Europe: a hospital-based survey. Lancet 377:63-73. http://dx.doi.org/10.1016/S0140-6736(10)61266-4.
43. Weber I, Riera E, Déniz C, Pérez JL, Oliver A, Mena A. 2013. Molecular epidemiology and resistance profiles of Clostridium difficile in a tertiary care hospital in Spain. Int. J. Med. Microbiol. 303:128-133. http://dx.doi.org/10.1016/j.ijmm.2013.02.016.
44. Schneeberg A, Rupnik M, Neubauer H, Seyboldt C. 2012. Prevalence and distribution of Clostridium difficile PCR ribotypes in cats and dogs from animal shelters in Thuringia, Germany. Anaerobe 18:484-488. http://dx.doi.org/10.1016/j.anaerobe.2012.08.002.
45. Zidaric V, Pardon B, Vultos Dos T, Deprez P, Brouwer MSM, Roberts AP, Henriques AO, Rupnik M. 2012. Different antibiotic resistance and sporulation properties within multiclonal Clostridium difficile PCR ribotypes 078, 126, and 033 in a single calf farm. Appl. Environ. Microbiol. 78:8515-8522. http://dx.doi.org/10.1128/AEM.02185-12.
46. Taori SK, Hall V, Poxton IR. 2010. Changes in antibiotic susceptibility and ribotypes in Clostridium difficile isolates from southern Scotland, 1979-2004. J. Med. Microbiol. 59:338-344. http://dx.doi.org/10.1099/jmm.0.014829-0.
47. Kurka H, Ehrenreich A, Ludwig W, Monot M, Rupnik M, Barbut F, Indra A, Dupuy B, Liebl W. 2014. Sequence similarity of Clostridium difficile strains by analysis of conserved genes and genome content is reflected by their ribotype affiliation. PLoS One 9:e86535. http://dx.doi.org/10.1371/journal.pone.0086535.
48. Muniesa M, Hammerl JA, Hertwig S, Appel B, Brüssow H. 2012. Shiga toxin-producing Escherichia coli O104:H4: a new challenge for microbiology. Appl. Environ. Microbiol. 78:4065-4073. http://dx.doi.org/10.1128/AEM.00217-12.
49. Goh S, Chang BJ, Riley TV. 2005. Effect of phage infection on toxin production by Clostridium difficile. J. Med. Microbiol. 54:129-135. http://dx.doi.org/10.1099/jmm.0.45821-0.
50. Bakker D, Corver J, Harmanus C, Goorhuis A, Keessen EC, Fawley WN, Wilcox MH, Kuijper EJ. 2010. Relatedness of human and animal Clostridium difficile PCR ribotype 078 isolates determined on the basis of multilocus variable-number tandem-repeat analysis and tetracycline resistance. J. Clin. Microbiol. 48:3744-3749. http://dx.doi.org/10.1128/JCM.01171-10.
51. Goorhuis A, Debast S, van Leengoed L, Harmanus C, Notermans D, Bergwerff A, Kuijper E, Songer J. 2008. Clostridium difficile PCR ribotype 078: an emerging strain in humans and in pigs? J. Clin. Microbiol. 46: 1157-1158. http://dx.doi.org/10.1128/JCM.01536-07.
52. Keel K, Brazier JS, Post KW, Weese S, Songer JG. 2007. Prevalence of PCR ribotypes among Clostridium difficile isolates from pigs, calves, and other species. J. Clin. Microbiol. 45:1963-1964. http://dx.doi.org/10.1128/JCM.00224-07.
53. Rodriguez-Palacios A, Staempfli HR, Duffield T, Weese JS. 2007. Clostridium difficile in retail ground meat, Canada. Emerging Infect. Dis. 13: 485-487. http://dx.doi.org/10.3201/eid1303.060988.
54. Weese JS, Avery BP, Rousseau J, Reid-Smith RJ. 2009. Detection and enumeration of Clostridium difficile spores in retail beef and pork. Appl. Environ. Microbiol. 75:5009-5011. http://dx.doi.org/10.1128/AEM.004 80-09.
55. Labrie SJ, Samson JE, Moineau S. 2010. Bacteriophage resistance mechanisms. Nat.Rev.Microbiol.8:317-327.http://dx.doi.org/10.1038/nrmicro 2315.
56. Rupnik M. 2010. Clostridium difficile: (re)emergence of zoonotic potential. Clin. Infect. Dis. 51:583-584. http://dx.doi.org/10.1086/655693.
57. Witte W. 2000. Selective pressure by antibiotic use in livestock. Int. J. Antimicrob. Agents 16(Suppl 1):S19-S24.
58. Goh S, Hussain H, Chang BJ, Emmett W, Riley TV, Mullany P. 2013. Phage φC2 mediates transduction of Tn6215, encoding erythromycin resistance, between Clostridium difficile strains. mBio 4:e00840-13. http://dx.doi.org/10.1128/mBio.00840-13.
59. Modi SR, Lee HH, Spina CS, Collins JJ. 2013. Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 499:219-222. http://dx.doi.org/10.1038/nature 12212.