Combined use of bacteriophage K and a novel bacteriophage to reduce Staphylococcus aureus biofilm formation

Applied and Environmental Microbiology

Volumn 80, Issue 21, 2014, Pages 6694-6703

  Alves, D R ^a   Gaudion, A ^a   Bean, J E ^a   Perez Esteban, P ^b   Arnot, T C ^b   Harper, D R ^c   Kot, W ^d   Hansen, L H ^d,e   Enright, M C ^a   Jenkins, A Tobias A ^a  

^a University of Bath Claverton Down   (United Kingdom)

^b University of Bath   (United Kingdom)

^c AmpliPhi Biosciences Corp   (United Kingdom)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BACTERIOPHAGES; ENZYME INHIBITION; MIXTURES;

BIOFILM BIOMASS; BIOFILM FORMATION; DOUBLE-STRANDED DNA (DS-DNA); PATIENT MORBIDITY; STAPHYLOCOCCUS AUREUS; VIRULENCE FACTORS; WOUND HEALING; WOUND PATHOGENS;

BIOFILMS;

BACTERIOPHAGE; BIOFILM; CLONE; DNA; GENOME; HOST RANGE; LYSIS; MORBIDITY; MORPHOLOGY; PATHOGEN; YEAST;

STAPHYLOCOCCUS AUREUS;

VIRUS DNA;

BACTERIOLYSIS; BIOFILM; CHEMISTRY; DNA SEQUENCE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST RANGE; MOLECULAR GENETICS; MYOVIRIDAE; PHYSIOLOGY; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS PHAGE; ULTRASTRUCTURE; VIROLOGY; VIRUS LOAD;

BACTERIOLYSIS; BIOFILMS; DNA, VIRAL; HOST SPECIFICITY; MOLECULAR SEQUENCE DATA; MYOVIRIDAE; SEQUENCE ANALYSIS, DNA; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS PHAGES; VIRAL LOAD;

EID: 84914140039     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01789-14     Document Type: Article

References (66)

1. Lowy FD. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339: 520-532. http://dx.doi.org/10.1056/NEJM199808203390806.
2. Foster TJ. 2005. Immune evasion by staphylococci. Nat. Rev. Microbiol. 3:948-958. http://dx.doi.org/10.1038/nrmicro1289.
3. Plata K, Rosato AE, Wegrzyn G. 2009. Staphylococcus aureus as an infectious agent: overview of biochemistry and molecular genetics of its pathogenicity. Acta Biochim. Pol. 56:597-612.
4. Chang S, Sievert DM, Hageman JC, Boulton ML, Tenover FC, Downes FP, Shah S, Rudrik JT, Pupp GR, Brown WJ, Cardo D, Fridkin SK. 2003. Infection with vancomycin-resistant Staphylococcus aureus containing the vanA resistance gene. N. Engl. J. Med. 348:1342-1347. http://dx.doi.org/10.1056/NEJMoa025025.
5. Murray CK, Holmes RL, Ellis MW, Mende K, Wolf SE, McDougal LK, Guymon CH, Hospenthal DR. 2009. Twenty-five year epidemiology of invasive methicillin-resistant Staphylococcus aureus (MRSA) isolates recovered at a burn center. Burns 35:1112-1117. http://dx.doi.org/10.1016/j.burns.2009.02.013.
6. Keen EF, Robinson BJ, Hospenthal DR, Aldous WK, Wolf SE, Chung KK, Murray CK. 2010. Prevalence of multidrug-resistant organisms recovered at a military burn center. Burns 36:819-825. http://dx.doi.org/10.1016/j.burns.2009.10.013.
7. Erol S, Altoparlak U, Akcay MN, Celebi F, Parlak M. 2004. Changes of microbial flora and wound colonization in burned patients. Burns 30: 357-361. http://dx.doi.org/10.1016/j.burns.2003.12.013.
8. Percival SL, Hill KE, Williams DW, Hooper SJ, Thomas DW, Costerton JW. 2012. A review of the scientific evidence for biofilms in wounds. Wound Repair Regen. 20:647-657. http://dx.doi.org/10.1111/j.1524-475X.2012.00836.x.
9. Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. 2010. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 35:322-332. http://dx.doi.org/10.1016/j.ijantimicag.2009.12.011.
10. De Beer D, Stoodley P, Lewandowski Z. 1997. Measurement of local diffusion coefficients in biofilms by microinjection and confocal microscopy. Biotechnol. Bioeng. 53:151-158. http://dx.doi.org/10.1002/(SICI)1097-0290(19970120)53:2 <151::AID-BIT4>3.0.CO;2-N.
11. Lam J, Chan R, Lam K, Costerton JW. 1980. Production of mucoid microcolonies by Pseudomonas aeruginosa within infected lungs in cystic fibrosis. Infect. Immun. 28:546-556.
12. James GA, Swogger E, Wolcott R, Pulcini ED, Secor P, Sestrich J, Costerton JW, Stewart PS. 2008. Biofilms in chronic wounds. Wound Repair Regen. 16:37-44. http://dx.doi.org/10.1111/j.1524-475X.2007.00321.x.
13. Davies CE, Hill KE, Wilson MJ, Stephens P, Hill CM, Harding KG, Thomas DW. 2004. Use of 16S ribosomal DNA PCR and denaturing gradient gel electrophoresis for analysis of the microfloras of healing and nonhealing chronic venous leg ulcers. J. Clin. Microbiol. 42:3549-3557. http://dx.doi.org/10.1128/JCM.42.8.3549-3557.2004.
14. Donlan RM. 2008. Biofilms on central venous catheters: is eradication possible? Curr. Top. Microbiol. Immunol. 322:133-161.
15. Darouiche RO. 2004. Treatment of infections associated with surgical implants. N. Engl. J. Med. 350:1422-1429. http://dx.doi.org/10.1056/NEJMra035415.
16. Sen CK, Gordillo GM, Roy S, Kirsner R, Lambert L, Hunt TK, Gottrup F, Gurtner GC, Longaker MT. 2010. Human skin wounds: a major and snowballing threat to public health and the economy. Wound Repair Regen. 17:763-771. http://dx.doi.org/10.1111/j.1524-475X.2009.00543.x.
17. Liapikou A, Torres A. 2013. Emerging drugs on methicillin-resistant Staphylococcus aureus. Expert Opin. Emerg. Drugs 18:291-305. http://dx.doi.org/10.1517/14728214.2013.813480.
18. Kurlenda J, Grinholc M. 2012. Alternative therapies in Staphylococcus aureus diseases. Acta Biochim. Pol. 59:171-184.
19. Burrowes B, Harper DR, Anderson J, McConville M, Enright MC. 2011. Bacteriophage therapy: potential uses in the control of antibiotic-resistant pathogens. Expert Rev. Anti Infect. Ther. 9:775-785. http://dx.doi.org/10.1586/eri.11.90.
20. Young I, Wang I, Roof WD. 2000. Phages will out: strategies of host cell lysis. Trends Microbiol. 8:120-128. http://dx.doi.org/10.1016/S0966-842X(00)01705-4.
21. Kraushaar B, Thanh MD, Hammerl JA, Reetz J, Fetsch A, Hertwig S. 2013. Isolation and characterization of phages with lytic activity against methicillin-resistant Staphylococcus aureus strains belonging to clonal complex 398. Arch. Virol. 158:2341-2350. http://dx.doi.org/10.1007/s00705-013-1707-6.
22. Capparelli R, Parlato M, Borriello G, Salvatore P, Iannelli D. 2007. Experimental phage therapy against Staphylococcus aureus in mice. Antimicrob. Agents Chemother. 51:2765-2773. http://dx.doi.org/10.1128/AAC.01513-06.
23. Gupta R, Prasad Y. 2011. Efficacy of polyvalent bacteriophage P-27/HP to control multidrug resistant Staphylococcus aureus associated with human infections. Curr. Microbiol. 62:255-260. http://dx.doi.org/10.1007/s00284-010-9699-x.
24. Abedon ST. 2011. Bacteriophages and biofilms: ecology, phage therapy, plaques. Nova Science Publishers, Hauppauge, NY.
25. Górski A, Miedzybrodzki R, Borysowski J, Weber-Dabrowska B, Lobocka M, Fortuna W, Letkiewicz S, Zimecki M, Filby G. 2009. Bacteriophage therapy for the treatment of infections. Curr. Opin. Investig. Drugs 10:766-774.
26. Skurnik M, Pajunen M, Kiljunen S. 2007. Biotechnological challenges of phage therapy. Biotechnol. Lett. 29:995-1003. http://dx.doi.org/10.1007/s10529-007-9346-1.
27. O'Flaherty S, Ross RP, Meaney W, Fitzgerald GF, Elbreki MF, Coffey A. 2005. Potential of the polyvalent anti-Staphylococcus bacteriophage K for control of antibiotic-resistant staphylococci from hospitals. Appl. Environ. Microbiol. 71:1836-1842. http://dx.doi.org/10.1128/AEM.71.4.1836-1842.2005.
28. Kelly D, McAuliffe O, Ross RP, Coffey A. 2012. Prevention of Staphylococcus aureus biofilm formation and reduction in established biofilm density using a combination of phage K and modified derivatives. Lett. Appl. Microbiol. 54:286-291. http://dx.doi.org/10.1111/j.1472-765X.2012.03205.x.
29. O'Flaherty S, Coffey A, Edwards R, Meaney W, Fitzgerald GF, Ross RP. 2004. Genome of staphylococcal phage K: a new lineage of Myoviridae infecting gram-positive bacteria with a low G+C content. J. Bacteriol. 186:2862-2871. http://dx.doi.org/10.1128/JB.186.9.2862-2871.2004.
30. Xia G, Corrigan RM, Winstel V, Goerke C, Gründling A, Peschel A. 2011. Wall teichoic acid-dependent adsorption of staphylococcal siphovirus and myovirus. J. Bacteriol. 193:4006-4009. http://dx.doi.org/10.1128/JB.01412-10.
31. Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG. 2000. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J. Clin. Microbiol. 38:1008-1015.
32. Tucker RG. 1961. The role of magnesium ions in the growth of Salmonella phage anti-R. J. Gen. Microbiol. 26:313-323. http://dx.doi.org/10.1099/00221287-26-2-313.
33. Adams M. 1959. Bacteriophages. Interscience Publishers, New York, NY.
34. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O. 2008. The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. http://dx.doi.org/10.1186/1471-2164-9-75.
35. Nirmal Kumar GP, Sundarrajan S, Paul VD, Nandini S, Saravanan RS, Hariharan S, Sriram B, Padmanabhan S. 2012. Use of prophage free host for achieving homogenous population of bacteriophages: new findings. Virus Res. 169:182-187. http://dx.doi.org/10.1016/j.virusres.2012.07.026.
36. 3-12, specific for Yersinia enterocolitica serotype O:3, is related to coliphages T3 and T7. J. Bacteriol. 182:5114-5120. http://dx.doi.org/10.1128/JB.182.18.5114-5120.2000.
37. Boulanger P. 2009. Purification of bacteriophages and SDS-PAGE analysis of phage structural proteins from ghost particles. Methods Mol. Biol. 502:227-238. http://dx.doi.org/10.1007/978-1-60327-565-1_13.
38. Pickard DJJ. 2009. Preparation of bacteriophage lysates and pure DNA. Methods Mol. Biol. 502:3-9. http://dx.doi.org/10.1007/978-1-60327-565-1_1.
39. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed, vol 1 to 3. CSH Press, Cold Spring Harbor, NY.
40. Kot W, Vogensen FK, Sørensen SJ, Hansen LH. 2014. DPS-a rapid method for genome sequencing of DNA-containing bacteriophages directly from a single plaque. J. Virol. Methods 196:152-156. http://dx.doi.org/10.1016/j.jviromet.2013.10.040.
41. Cerca N, Oliveira R, Azeredo J. 2007. Susceptibility of Staphylococcus epidermidis planktonic cells and biofilms to the lytic action of staphylococcus bacteriophage K. Lett. Appl. Microbiol. 45:313-317. http://dx.doi.org/10.1111/j.1472-765X.2007.02190.x.
42. Abramson JH. 2011. WINPEPI updated: computer programs for epidemiologists, and their teaching potential. Epidemiol. Perspect. Innov. 8:1. http://dx.doi.org/10.1186/1742-5573-8-1.
43. Sillankorva S, Neubauer P, Azeredo J. 2008. Isolation and characterization of a T7-like lytic phage for Pseudomonas fluorescens. BMC Biotechnol. 8:80. http://dx.doi.org/10.1186/1472-6750-8-80.
44. Ackermann H-W. 2011. Bacteriophage taxonomy. Microbiol. Aust. 32: 90-94.
45. Rees PJ, Fry BA. 1981. The morphology of staphylococcal bacteriophage K and DNA metabolism in infected Staphylococcus aureus. J. Gen. Virol. 53:293-307. http://dx.doi.org/10.1099/0022-1317-53-2-293.
46. Streisinger G, Emrich J, Stahl MM. 1967. Chromosome structure in phage t4, iii. Terminal redundancy and length determination. Proc. Natl. Acad. Sci. U. S. A. 57:292-295. http://dx.doi.org/10.1073/pnas.57.2.292.
47. Kwan T, Liu J, DuBow M, Gros P, Pelletier J. 2005. The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Proc. Natl. Acad. Sci. U. S. A. 102:5174-5179. http://dx.doi.org/10.1073/pnas.0501140102.
48. Cui Z, Song Z, Wang Y, Zeng L, Shen W, Wang Z, Li Q, He P, Qin J, Guo X. 2012. Complete genome sequence of wide-host-range Staphylococcus aureus phage JD007. J. Virol. 86:13880-13881. http://dx.doi.org/10.1128/JVI.02728-12.
49. Gu J, Liu X, Lu R, Li Y, Song J, Lei L, Sun C, Feng X, Du C, Yu H, Yang Y, Han W. 2012. Complete genome sequence of Staphylococcus aureus bacteriophage GH15. J. Virol. 86:8914-8915. http://dx.doi.org/10.1128/JVI.01313-12.
50. Deghorain M, Van Melderen L. 2012. The staphylococci phages family: an overview. Viruses 4:3316-3335. http://dx.doi.org/10.3390/v4123316.
51. Łobocka M, Hejnowicz Dabrowski MS, Gozdek K, Kosakowski A, Witkowska J, Ulatowska MI, Weber-Dabrowska B, Kwiatek M, Parasion S, Gawor J, Kosowska H, Głowacka A. 2012. Genomics of staphylococcal Twort-like phages-potential therapeutics of the postantibiotic era. Adv. Virus Res. 83:143-216. http://dx.doi.org/10.1016/B978-0-12-394438-2.00005-0.
52. Hsieh S-E, Lo H-H, Chen S-T, Lee M-C, Tseng Y-H. 2011. Wide host range and strong lytic activity of Staphylococcus aureus lytic phage Stau2. Appl. Environ. Microbiol. 77:756-761. http://dx.doi.org/10.1128/AEM.01848-10.
53. Kwiatek M, Parasion S, Mizak L, Gryko R, Bartoszcze M, Kocik J. 2012. Characterization of a bacteriophage, isolated from a cow with mastitis, that is lytic against Staphylococcus aureus strains. Arch. Virol. 157:225-234. http://dx.doi.org/10.1007/s00705-011-1160-3.
54. Hejkal TW, Wellings FM, Lewis AL, LaRock PA. 1981. Distribution of viruses associated with particles in waste water. Appl. Environ. Microbiol. 41:628-634.
55. Narang HK, Codd AA. 1981. Frequency of preclumped virus in routine fecal specimens from patients with acute nonbacterial gastroenteritis. J. Clin. Microbiol. 13:982-988.
56. Langlet J, Gaboriaud F, Gantzer C. 2007. Effects of pH on plaque forming unit counts and aggregation of MS2 bacteriophage. J. Appl. Microbiol. 103:1632-1638. http://dx.doi.org/10.1111/j.1365-2672.2007.03396.x.
57. Zemb O, Manefield M, Thomas F, Jacquet S. 2013. Phage adsorption to bacteria in the light of the electrostatics: a case study using E. coli, T2 and flow cytometry. J. Virol. Methods 189:283-289. http://dx.doi.org/10.1016/j.jviromet.2013.02.007.
58. Esteban PP, Alves DR, Enright MC, Bean JE, Gaudion A, Jenkins ATA, Young AER, Arnot TC. 2014. Enhancement of the antimicrobial properties of bacteriophage-K via stabilization using oil-in-water nanoemulsions. Biotechnol. Prog. 30:932-944. http://dx.doi.org/10.1002/btpr.1898.
59. Hatfull GF. 2008. Bacteriophage genomics. Curr. Opin. Microbiol. 11: 447-453. http://dx.doi.org/10.1016/j.mib.2008.09.004.
60. Lima-Mendez G, Toussaint A, Leplae R. 2011. A modular view of the bacteriophage genomic space: identification of host and lifestyle markermodules. Res. Microbiol. 162:737-746. http://dx.doi.org/10.1016/j.resmic.2011.06.006.
61. Tanji Y, Shimada T, Fukudomi H, Miyanaga K, Nakai Y, Unno H. 2005. Therapeutic use of phage cocktail for controlling Escherichia coli O157:H7 in gastrointestinal tract of mice. J. Biosci. Bioeng. 100:280-287. http://dx.doi.org/10.1263/jbb.100.280.
62. Gu J, Liu X, Li Y, Han W, Lei L, Yang Y, Zhao H, Gao Y, Song J, Lu R, Sun C, Feng X. 2012. A method for generation phage cocktail with great therapeutic potential. PLoS One 7:e31698. http://dx.doi.org/10.1371/journal.pone.0031698.
63. Ryan EM, Alkawareek MY, Donnelly RF, Gilmore BF. 2012. Synergistic phage-antibiotic combinations for the control of Escherichia coli biofilms in vitro. FEMS Immunol. Med. Microbiol. 65:395-398. http://dx.doi.org/10.1111/j.1574-695X.2012.00977.x.
64. Comeau AM, Tétart F, Trojet SN, Prère M-F, Krisch HM. 2007. Phageantibiotic synergy (PAS): beta-lactam and quinolone antibiotics stimulate virulent phage growth. PLoS One 2:e799. http://dx.doi.org/10.1371/journal.pone.0000799.
65. Kirby AE. 2012. Synergistic action of gentamicin and bacteriophage in a continuous culture population of Staphylococcus aureus. PLoS One 7:e51017. http://dx.doi.org/10.1371/journal.pone.0051017.
66. Henein A. 2013. What are the limitations on the wider therapeutic use of phage? Bacteriophage 3:e24872. http://dx.doi.org/10.4161/bact.24872.