Three new Escherichia coli phages from the human gut show promising potential for phage therapy

PLoS ONE

Volumn 11, Issue 6, 2016, Pages

  Dalmasso, Marion ^a,b,e   Strain, Ronan ^a,b   Neve, Horst ^c   Franz, Charles M A P ^c   Cousin, Fabien J ^a,b,e   Ross, R Paul ^b,d   Hill, Colin ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c FEDERAL RESEARCH INSTITUTE OF NUTRITION AND FOOD   (Germany)

^d TEAGASC FOOD RESEARCH CENTRE   (Ireland)

^e UNIVERSITÉ DE CAEN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CIPROFLOXACIN;

ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BIOFILM; COLIPHAGE; CONTROLLED STUDY; ESCHERICHIA COLI; GROWTH INHIBITION; HOST RANGE; INTESTINE FLORA; MICROBIAL POPULATION DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; ESCHERICHIA COLI INFECTION; FECES; GASTROINTESTINAL TRACT; GROWTH, DEVELOPMENT AND AGING; HUMAN; MICROBIOLOGY; PHAGE THERAPY;

BIOFILMS; COLIPHAGES; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FECES; GASTROINTESTINAL TRACT; GENOME, BACTERIAL; HUMANS; PHAGE THERAPY;

EID: 84976276828     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0156773     Document Type: Article

References (61)

1. Tarr PI. Escherichia coli O157:H7: clinical, diagnostic, and epidemiological aspects of human infection. Clin Infect Dis. 1995; 20(1):1-8. PMID: 7727633.
2. Rahal EA, Fadlallah SM, Nassar FJ, Kazzi N, Matar GM. Approaches to treatment of emerging shiga toxin-producing Escherichia coli infections highlighting the O104:H4 serotype. Fron Cell Infect Microbiol. 2015; 5:24. doi: 10.3389/fcimb.2015.00024 PMID: 25853096.
3. Hu J, Torres AG. Enteropathogenic Escherichia coli: foe or innocent bystander? Clin Microbiol Infect. 2015; doi: 10.1016/j.cmi.2015.01.015 PMID: 25726041.
4. Ansari S, Nepal HP, Gautam R, Shrestha S, Neopane P, Gurung G, et al. Community acquired multidrug resistant clinical isolates of Escherichia coli in a tertiary care center of Nepal. Antimicrob Resist Infect Control. 2015; 4:15. doi: 10.1186/s13756-015-0059-2 PMID: 25937923.
5. Wittebole X, De Roock S, Opal SM. A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence. 2014; 4(1):1-10. doi: 10.4161/viru.25991 PMID: 23973944.
6. Viertel TM, Ritter K, Horz HP. Viruses versus bacteria-novel approaches to phage therapy as a tool against multidrug-resistant pathogens. J Antimicrob Chemother. 2014; 69(9):2326-36. doi: 10.1093/jac/dku173 WOS:000343322200004. PMID: 24872344
7. Endersen L, O'Mahoney J, Hill C, Ross RP, McAuliffe O, Coffey A. Phage therapy in the food industry. Annu Rev Food Sci Technol. 2014; 5(1):327-49. doi: 10.1146/annurev-food-030713-092415 PMID: 24422588.
8. Lu TK, Koeris MS. The next generation of bacteriophage therapy. Curr Opin Microbiol. 2011; 14 (5):524-31. doi: 10.1016/j.mib.2011.07.028 PMID: 21868281.
9. Cha SB, Yoo AN, Lee WJ, Shin MK, Jung MH, Shin SW, et al. Effect of bacteriophage in enterotoxigenic Escherichia coli (ETEC) infected pigs. J Vet Med Sci. 2012; 74(8):1037-9. PMID: 22446401.
10. Maura D, Galtier M, Le Bouguenec C, Debarbieux L. Virulent bacteriophages can target O104:H4 enteroaggregative Escherichia coli in the mouse intestine. Antimicrob Agents Chemother. 2012; 56 (12):6235-42. PMID: 23006754. doi: 10.1128/AAC.00602-12
11. Sarker SA, McCallin S, Barretto C, Berger B, Pittet AC, Sultana S, et al. Oral T4-like phage cocktail application to healthy adult volunteers from Bangladesh. Virology. 2012; 434(2):222-32. doi: 10.1016/j.virol.2012.09.002 PMID: 23102968.
12. Bruttin A, Brussow H. Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob Agents Chemother. 2005; 49(7):2874-8. doi: 10.1128/aac.49.7.2874-2878.2005 PMID: 15980363.
13. Cusack S, O'Toole PW. Challenges and implications for biomedical research and intervention studies in older populations: Insights from the ELDERMET study. Gerontology. 2013; 59(2):114-21. PMID: 23146954. doi: 10.1159/000343158
14. Claesson MJ, Jeffery IB, Conde S, Power SE, O'Connor EM, Cusack S, et al. Gut microbiota composition correlates with diet and health in the elderly. Nature. 2012; 488(7410):178-84. doi: 10.1038/ nature11319 PMID: 22797518.
15. Murphy J, Royer B, Mahony J, Hoyles L, Heller K, Neve H, et al. Biodiversity of lactococcal bacteriophages isolated from 3 Gouda-type cheese-producing plants. Journal of dairy science. 2013; 96 (8):4945-57. doi: 10.3168/jds.2013-6748 PMID: 23769356.
16. Chaudhuri RR, Sebaihia M, Hobman JL, Webber MA, Leyton DL, Goldberg MD, et al. Complete genome sequence and comparative metabolic profiling of the prototypical enteroaggregative Escherichia coli strain 042. PLoS One. 2010; 5(1):e8801. doi: 10.1371/journal.pone.0008801 PMID: 20098708.
17. Iguchi A, Thomson NR, Ogura Y, Saunders D, Ooka T, Henderson IR, et al. Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127:H6 strain E2348/69. J Bacteriol. 2009; 191(1):347-54. doi: 10.1128/jb.01238-08 PMID: 18952797.
18. Hayashi T, Makino K, Ohnishi M, Kurokawa K, Ishii K, Yokoyama K, et al. Complete genome sequence of enterohemorrhagic Eschelichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res. 2001; 8(1):11-22. doi: 10.1093/dnares/8.1.11 PMID: 11258796.
19. Crossman LC, Chaudhuri RR, Beatson SA, Wells TJ, Desvaux M, Cunningham AF, et al. A commensal gone bad: complete genome sequence of the prototypical enterotoxigenic Escherichia coli strain H10407. J Bacteriol. 2010; 192(21):5822-31. doi: 10.1128/jb.00710-10 PMID: 20802035.
20. Subramanian S, Rhodes JM, Hart CA, Tam B, Roberts CL, Smith SL, et al. Characterization of epithelial IL-8 response to inflammatory bowel disease mucosal E. coli and its inhibition by mesalamine. Inflamm Bowel Dis. 2008; 14(2):162-75. doi: 10.1002/ibd.20296 PMID: 17941093.
21. Hejnova J, Dobrindt U, Nemcova R, Rusniok C, Bomba A, Frangeul L, et al. Characterization of the flexible genome complement of the commensal Escherichia coli strain A0 34/86 (O83: K24: H31). Microbiol. 2005; 151(2):385-98. doi: 10.1099/mic.0.27469-0 PMID: 15699189.
22. Mulvey MA, Schilling JD, Hultgren SJ. Establishment of a persistent Escherichia coli reservoir during the acute phase of a bladder infection. Infect Immun. 2001; 69(7):4572-9. doi: 10.1128/iai.69.7.4572-4579.2001 PMID: 11402001.
23. Mobley HL, Green DM, Trifillis AL, Johnson DE, Chippendale GR, Lockatell CV, et al. Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. Infect Immun. 1990; 58(5):1281-9. PMID: 2182540.
24. O'Flaherty S, Coffey A, Meaney W, Fitzgerald GF, Ross RP. The recombinant phage lysin LysK has a broad spectrum of lytic activity against clinically relevant staphylococci, including methicillin-resistant Staphylococcus aureus. J Bacteriol. 2005; 187(20):7161-4. doi: 10.1128/JB.187.20.7161-7164.2005 PMC1251611. PMID: 16199588
25. Casey E, Mahony J, Neve H, Noben JP, Dal Bello F, van Sinderen D. Novel phage group infecting Lactobacillus delbrueckii subsp. lactis, as revealed by genomic and proteomic analysis of bacteriophage Ldl1. Appl Environ Microbiol. 2015; 81(4):1319-26. doi: 10.1128/aem.03413-14 PMID: 25501478.
26. Tunney MM, Ramage G, Field TR, Moriarty TF, Storey DG. Rapid colorimetric assay for antimicrobial susceptibility testing of Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2004; 48(5):1879-81. PMID: 15105149.
27. Field D, Gaudin N, Lyons F, O'Connor PM, Cotter PD, Hill C, et al. A bioengineered nisin derivative to control biofilms of Staphylococcus pseudintermedius. PLoS One. 2015; 10(3):e0119684. doi: 10.1371/journal.pone.0119684 PMID: 25789988.
28. Baron F, Cochet M-F, Ablain W, Grosset N, Madec M-N, Gonnet F, et al. Rapid and cost-effective method for micro-organism enumeration based on miniaturization of the conventional plate-counting technique. Lait. 2006; 86(3):251-7.
29. Hoyles L, McCartney AL, Neve H, Gibson GR, Sanderson JD, Heller KJ, et al. Characterization of virus-like particles associated with the human faecal and caecal microbiota. Res Microbiol. 2014; 165 (10):803-12. doi: 10.1016/j.resmic.2014.10.006 PMID: 25463385.
30. Delcher AL, Harmon D, Kasif S, White O, Salzberg SL. Improved microbial gene identification with GLIMMER. Nucleic Acids Res. 1999; 27(23):4636-41. PMID: 10556321.
31. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997; 25 (17):3389-402. PMID: 9254694.
32. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 2014; 42:D206-14. doi: 10.1093/nar/gkt1226 PMID: 24293654.
33. Laslett D, Canback B. ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res. 2004; 32(1):11-6. doi: 10.1093/nar/gkh152 PMID: 14704338.
34. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics. 2011; 12:402. doi: 10.1186/1471-2164-12-402 PMID: 21824423.
35. Dalmasso M, Hill C, Ross RP. Exploiting gut bacteriophages for human health. Trends Microbiol. 2014; 22(7):399-405. doi: 10.1016/j.tim.2014.02.010 PMID: 24656964.
36. Jeffery IB, Lynch DB, O'Toole PW. Composition and temporal stability of the gut microbiota in older persons. ISME J. 2016; 10(1):170-82. doi: 10.1038/ismej.2015.88 PMID: 26090993
37. Yap ML, Rossmann MG. Structure and function of bacteriophage T4. Future Microbiol. 2014; 9 (12):1319-37. doi: 10.2217/fmb.14.91 WOS:000346478500004. PMID: 25517898
38. Truncaite L, Simoliunas E, Zajanckauskaite A, Kaliniene L, Mankeviciute R, Staniulis J, et al. Bacteriophage vB-EcoM-FV3: a new member of "rV5-like viruses". Arch Virol. 2012; 157(12):2431-5. doi: 10.1007/s00705-012-1449-x PMID: 22907825.
39. Kropinski AM, Waddell T, Meng J, Franklin K, Ackermann HW, Ahmed R, et al. The host-range, genomics and proteomics of Escherichia coli O157:H7 bacteriophage rV5. Virol J. 2013; 10:76. doi: 10.1186/1743-422x-10-76 PMID: 23497209.
40. Kim M, Ryu S. Characterization of a T5-like coliphage, SPC35, and differential development of resistance to SPC35 in Salmonella enterica serovar typhimurium and Escherichia coli. Appl Environ Microbiol. 2011; 77(6):2042-50. doi: 10.1128/aem.02504-10 PMID: 21257810.
41. Mahony J, McAuliffe O, Ross RP, van Sinderen D. Bacteriophages as biocontrol agents of food pathogens. Curr Opin Biotechnol. 2011; 22(2):157-63. doi: 10.1016/j.copbio.2010.10.008 PMID: 21115341.
42. Dufour N, Debarbieux L, Fromentin M, Ricard JD. Treatment of highly virulent extraintestinal pathogenic Escherichia coli pneumonia with bacteriophages. Crit Care Med. 2015; 43(6):e190-8. PMID: 25803649.
43. Rahmani R, Zarrini G, Sheikhzadeh F, Aghamohammadzadeh N. Effective phages as green antimicrobial agents against antibiotic-resistant hospital Escherichia coli. Jundishapur J Microbiol. 2015; 8(2): e17744. doi: 10.5812/jjm.17744 PMID: 25834712.
44. Holt KE, Baker S, Weill FX, Holmes EC, Kitchen A, Yu J, et al. Shigella sonnei genome sequencing and phylogenetic analysis indicate recent global dissemination from Europe. Nat Genet. 2012; 44(9):1056-9. doi: 10.1038/ng.2369 PMID: 22863732.
45. Chang HW, Kim KH. Comparative genomic analysis of bacteriophage EP23 infecting Shigella sonnei and Escherichia coli. J Microbiol. 2011; 49(6):927-34. doi: 10.1007/s12275-011-1577-0 PMID: 22203555.
46. Abedon ST. Lysis from without. Bacteriophage. 2011; 1(1):46-9. doi: 10.4161/bact.1.1.13980 PMC3109453. PMID: 21687534
47. Khan Mirzaei M, Nilsson AS. Isolation of phages for phage therapy: a comparison of spot tests and efficiency of plating analyses for determination of host range and efficacy. PLoS One. 2015; 10(3): e0118557. doi: 10.1371/journal.pone.0118557 PMID: 25761060.
48. Lu Z, Breidt F. Escherichia coli O157:H7 bacteriophage Phi241 isolated from an industrial cucumber fermentation at high acidity and salinity. Front Microbiol. 2015; 6:67. doi: 10.3389/fmicb.2015.00067 PMID: 25741324.
49. Brussow H. What is needed for phage therapy to become a reality in Western medicine? Virology. 2012; 434(2):138-42. doi: 10.1016/j.virol.2012.09.015 PMID: 23059181.
50. Tang F, Li Y, Zhang W, Lu C. Complete genome sequence of T4-Like Escherichia coli bacteriophage HX01. J Virol. 2012; 86(24):13871. doi: 10.1128/jvi.02698-12 PMID: 23166268.
51. Tsonos J, Oosterik LH, Tuntufye HN, Klumpp J, Butaye P, De Greve H, et al. A cocktail of in vitro efficient phages is not a guarantee for in vivo therapeutic results against avian colibacillosis. Vet Microbiol. 2014; 171(3-4):470-9. doi: 10.1016/j.vetmic.2013.10.021 PMID: 24269008.
52. Brüssow H. Phage therapy: the Escherichia coli experience. Microbiol. 2005; 151(7):2133-40. doi: 10.1099/mic.0.27849-0
53. Denou E, Bruttin A, Barretto C, Ngom-Bru C, Brussow H, Zuber S. T4 phages against Escherichia coli diarrhea: potential and problems. Virology. 2009; 388(1):21-30. doi: 10.1016/j.virol.2009.03.009 PMID: 19339031.
54. Hatfull GF, Hendrix RW. Bacteriophages and their genomes. Curr Opin Virol. 2011; 1(4):298-303. doi: 10.1016/j.coviro.2011.06.009 PMID: 22034588.
55. Kim M, Ryu S. Characterization of a T5-like coliphage, SPC35, and differential development of resistance to SPC35 in Salmonella enterica serovar Typhimurium and Escherichia coli. Appl Environ Microbiol. 2011; 77(6):2042-50. doi: 10.1128/aem.02504-10 PMID: 21257810.
56. Parasion S, Kwiatek M, Gryko R, Mizak L, Malm A. Bacteriophages as an alternative strategy for fighting biofilm development. Polish J Microbiol. 2014; 63(2):137-45. PMID: 25115107.
57. O'Flynn G, Ross RP, Fitzgerald GF, Coffey A. Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157:H7. Appl Environ Microbiol. 2004; 70(6):3417-24. doi: 10.1128/aem.70.6.3417-3424.2004 PMID: 15184139.
58. Ly-Chatain MH. The factors affecting effectiveness of treatment in phages therapy. Front Microbiol. 2014; 5:51. doi: 10.3389/fmicb.2014.00051 PMID: 24600439.
59. Coulter LB, McLean RJ, Rohde RE, Aron GM. Effect of bacteriophage infection in combination with tobramycin on the emergence of resistance in Escherichia coli and Pseudomonas aeruginosa biofilms. Viruses. 2014; 6(10):3778-86. doi: 10.3390/v6103778 PMID: 25285538.
60. Comeau AM, Tétart F, Trojet SN, Prère M-F, Krisch HM. Phage-Antibiotic Synergy (PAS): β-Lactam and quinolone antibiotics stimulate virulent phage growth. PLoS One. 2007; 2(8):e799. doi: 10.1371/journal.pone.0000799 PMID: 17726529.
61. Kamal F, Dennis JJ. Burkholderia cepacia complex Phage-Antibiotic Synergy (PAS): antibiotics stimulate lytic phage activity. Appl Environ Microbiol. 2015; 81(3):1132-8. doi: 10.1128/aem.02850-14 PMID: 25452284.