Bacteriophages and its applications: an overview

Folia Microbiologica

Volumn 62, Issue 1, 2017, Pages 17-55

  Sharma, Sonika ^a   Chatterjee, Soumya ^a   Datta, Sibnarayan ^a   Prasad, Rishika ^a,b   Dubey, Dharmendra ^a   Prasad, Rajesh Kumar ^a   Vairale, Mohan G ^a  

^a Defence R D Organization   (India)

^b Cornell University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL INFECTIONS; BACTERIOPHAGE; BIOTECHNOLOGY; CLASSIFICATION; HUMAN; MEDICAL RESEARCH; PHAGE THERAPY; PHYSIOLOGY; PROCEDURES; TRENDS;

BACTERIAL INFECTIONS; BACTERIOPHAGES; BIOMEDICAL RESEARCH; BIOTECHNOLOGY; HUMANS; PHAGE THERAPY;

EID: 84990891487     PISSN: 00155632     EISSN: 18749356     Source Type: Journal    
DOI: 10.1007/s12223-016-0471-x     Document Type: Review

References (237)

1. Abedon ST (2016) Bacteriophage exploitation of bacterial biofilms: phage preference for less mature targets? FEMS Microbiol Lett. doi:10.1093/femsle/fnv246
2. Abedon ST, Herschler TD, Stopar D (2001) Bacteriophage latent-period evolution as a response to resource availability. Appl Environ Microbiol 13:4233–4241
3. Abedon ST, Sarah JK, Bob GB, Kutter EM (2011) Phage treatment of human infections. Bacteriophage. 1(2):66–85
4. Abeles AL, Snyder KM, Chattoraj DK (1984) P1 plasmid replication: replicon structure. J Mol Biol 17:307–324
5. Ackermann HW (2011a) Bacteriophage taxonomy Microbiology Australia, 90–94. Downloaded from http://journals.cambridgemedia.com.au/UserDir/CambridgeJournal/Articles/11%20ackermann244.pdf
6. Adriaenssens EM, Vaerenbergh JV, Vandenheuvel D (2012) T4-related bacteriophage LIMEstone isolates for the control of soft rot on potato caused by Dickeya solani. PLoS One 7:e33227
7. Alisky J, Iczkowski K, Rapoport A, Troitsky N (1998) Bacteriophages show promise as antimicrobial agents. J Infect 36:5–15
8. Allen HK, Looft T, Bayles DO, Humphrey S, Levine UY, Alt D, Stanton TB (2011) Antibiotics in feed induce prophages in swine fecal microbiomes. MBio 2:00260–00211
9. Allwood PB, Malik YS, Maherchandani S, Vought K, Johnson LA, Braymen C, Hedberg CW, Goyal SM (2004) Occurrence of Escherichia coli, noroviruses, and f-specific coliphages in fresh market-ready produce. J Food Protect 67:2387–2390
10. Almeida A, Cunha A, Gomes NCM, Alves E, Costa L et al (2009) Phage therapy and photodynamic therapy: low environmental impact approaches to inactivate microorganisms in fish farming plants. Mar Drugs 7:268–313
11. Atias D, Lobel L, Virta M, Marks RS (2008) Phage-displayed epitopes as bioreceptors for biosensors part two. Biological and molecular recognition systems. Wiley, Handbook of Biosensors and Biochips. doi:10.1002/9780470061565.hbb012
12. Babalova EG, Katsitadze KT, Sakvarelidze LA, Imnaishvili NS, Sharashidze TG, Badashvili VA, Kiknadze GP, Meĭpariani AN, Gendzekhadze ND, Machavariani EV, Gogoberidze KL, Gozalov EI, Dekanosidze NG (1968) Preventive value of dried dysentery bacteriophages. Zh Mikrobiol Epidemiol Immunobiol 45:143–145
13. Balasubramanian S, Sorokulova IB, Vodyanoy VJ, Simonian AL (2007) Lytic phage as a specific and selective probe for detection of Staphylococcus aureus—a surface plasmon resonance spectroscopic study. Biosens. Bioelectron. 22:948–955
14. Balogh B, Canteros BI, Stall RE, Jones JB (2008) Control of citrus canker and citrus bacterial spot with bacteriophages. Plant Dise 92:1048–1052
15. Balogh B, Jones JB, Momolet MT (2003) Improved efficacy of newly formulated bacteriophages for management of bacterial spot on tomato. Plant Dis 87:949–954
16. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–1712
17. Barry MA, Dower WJ, Johnston SA (1996) Toward cell-targeting gene therapy vectors: selection of cell-binding peptides from random peptide presenting phage libraries. Nat Med 2:299–305
18. Bell RG (1976) The limitation of the ratio of fecal coliform to total coliphage as a water pollution index. Water Res 10:745–748
19. Benhar I (2001) Biotechnological applications of phage and cell display. Biotechnol Adv 19:1–33
20. Bickle TA, Kruger DH (1993) Biology of DNA restriction. Microbiol Rev 57:434–450
21. Biswas B, Adhya S, Washart P, Paul B, Trostel AN, Powell B, Carlton R, Merril CR (2002) Bacteriophage therapy rescues mice bacteremic from a clinical isolate of vancomycin-resistant Enterococcus faecium. Infect Immun 70:204–210
22. Bolotin A, Ouinquis B, Sorokin A, Ehrlich SD (2005) Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151:2551–2561
23. Borgaro JG, Zhu Z (2013) Characterization of the 5-hydroxymethylcytosine-specific DNA restriction endonucleases. Nucleic Acids Res 41:4198–4206
24. Bradley DE (1967) Ultrastructure of bacteriophages and bacteriocins. Bacteriol Rev 31:230–314
25. Bradley DE, Kay D (1960) The fine structure of Bacteriophages. J Gen Microbiol 23:553–563
26. Breitbart M (2012) Marine viruses: truth or dare. Annu Rev Mar Sci 4:425–448
27. Breitbart M, Wegley L, Leeds S, Schoenfeld T, Rohwer F (2004) Phage community dynamics in hot springs. Appl Environ Microbiol 70:1633–1640
28. Brenner S, Horne RW (1959) A negative staining method for high-resolution electron microscopy of viruses. Biochim Biophys Acta 34:103–110. doi:10.1016/0006-3002(59)90237-9
29. Brenner S, Streisinger G, Horne RW, Champe SP, Barnett L, Benzer S, Rees MW (1959) Structural components of bacteriophage. J Mol Biol 1:281
30. Brock TD, Madigan, Michael T (1988) Biology of microorganisms, 5th edn. Prentice-Hall, USA, pp. 1988–1835
31. Brown S, Maria JPS, Walker S (2013) Wall teichoic acids of grampositive bacteria. In: S. Gottesman (ed) Annual Review of Microbiology, 67 (Palo Alto: Annual Reviews), pp 313–336
32. Brussow H, Canchaya C, Hardt W (2004) Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68:560–602
33. Bruttin A, Brüssow H (2005) Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob Agents Chemother 49:2874–2878
34. Bruynoghe R, Maisin J (1921) Essais de theârapeutique au moyen du bacteriophage. J Soc Biol 85:1120–1121
35. Bryson AL, Hwang Y, Sherrill-Mix S, Wu GD, Lewis JD, Black L, Clark TA, Bushman FD (2015) Covalent modification of bacteriophage T4 DNA inhibits CRISPR-Cas9. MBio 6:e00648. doi:10.1128/mBio.00648-15
36. Buckling A, Rainey PB (2002) Antagonistic coevolution between a bacterium and a bacteriophage. P Roy Soc B Biol Sci 269:931–936
37. Bugla-Ploskonska G, Futoma-Koloch B, Doroszkiewicz W (2007) Role of outer membrane proteins of gram-negative bacteria in interaction with human organism. Postepy Mikrobiol 46:139–152
38. Cademartiri R, Anany H, Gross I, Bhayani R, Griffiths M, Brook MA (2010) Immobilization of bacteriophages on modified silica particles. Biomaterials 31:1904–1910
39. Campbell NA, Reece JB (2005) Biology. Pearson, Benjamin Cummings, San Francisco, pp. 338–339
40. Chatterjee M, Anju CP, Biswas L, Anil Kumar V, Gopi Mohan C, Biswas R (2015) Antibiotic resistance in Pseudomonas aeruginosa and alternative therapeutic options. Int J Med Microbiol doi. doi:10.1016/j.ijmm.2015.11.004
41. Chuang CH, Wu TF, Chen CH, Chang KC, Ju JW, Huang YW, Van Nhan V (2015) Lab on a chip for multiplexed immunoassays to detect bladder cancer using multifunctional dielectrophoretic manipulations. Lab Chip 15:3056–3064
42. Clark JR, March JB (2004) Bacterial viruses as human vaccines? Expert Rev Vaccines 3:463–476
43. Crothers-Stomps C, Høj L, Bourne DG, Hall MR, Owens L (2010) Isolation of lytic bacteriophages against Vibrio harveyi. J Appl Microbiol 108:1744–1750
44. Cui Z (2015) Advances in the treatment of wound bacterial infection with phage. Zhonghua Shao Shang ZaZhi 31:389–391
45. D’Herelle F (1917a) Sur un microbe invisible antagoniste des bacillesdysente ´riques. C R Academy of Sciences (Paris) 165:373–375
46. D’Herelle F (1930) The bacteriophage and its clinical applications. Charles C Thomas, Springfield, Ill
47. Dalmasso M, Strain R, Neve H, Franz CMAP, Cousin FJ, Ross RP (2016) Three new Escherichia coli phages from the human gut show promising potential for phage therapy. PLoS One 11(6):e0156773. doi:10.1371/journal.pone.0156773
48. d’Herelle F (1917b) On an invisible microbe antagonistic to dysentery bacilli. Comptes Rendus Academie des Sciences 165:373–375
49. d’Herelle F (1949) The bacteriophage. Science News 14:44–59
50. Dickerson TJ, Kaufmann GF, Janda KD (2005) Bacteriophage-mediated protein delivery into the central nervous system and its application in immune pharmacotherapy. Expert Opin Biol Ther 5:773–781
51. Donnelly A, Yata T, Bentayebi K, Suwan K, Hajitou A (2015) Bacteriophage mediates efficient Gene transfer in combination with conventional Transfection reagents. Viruses 7:6476–6489
52. Duckworth DH (1976) Who discovered Bacteriophage? Bacteriol Rev 40:793–802
53. Duckworth DH, Gulig PA (2002) Bacteriophages: potential treatment for bacterial infections. BioDrugs 16:57–62
54. DuPont HL (2007) The growing threat of foodborne bacterial enteropathogens of animal origin. Clin Infect Dis 45:1353–1361
55. FAO Report (2015) Downloaded from: http://www.fao.org/3/a-i4910e.pdf. Accessed 09 Jan 2016
56. Fiorentin L, Vieira ND, Bavioni JW, Aves ES (2005) Use of lytic bacteriophages to reduce salmonella enteritidis in experimentally contaminated chicken cuts. Braz J Poult Sci 7:255–260
57. Flaherty JE, Jones JB, Harbaugh BK, Somodi GC, Jackson LE (2000) Control of bacterial spot on tomato in the greenhouse and field with h-mutant bacteriophages. Hort Sci 35:882–884
58. Flegel TW (2006) Detection of major penaeid shrimp viruses in Asia, a historical perspective with emphasis on Thailand. Aquaculture 258:1–33
59. Frampton RA, Pitman AR, Fineran PC (2012) Advances in Bacteriophage-mediated control of plant pathogens. Int J Microbiol Res. doi:10.1155/2012/326452Article ID 326452, 11 pages
60. Fu F, Wang Q (2011) Removal of heavy metal ions from wastewaters: a review. J. Environ Manag 92:407–418. doi:10.1016/j.jenvman.2010.11.011
61. Fujiwara A, Fujisawa M, Hamasaki R, Kawasaki T, Fujie M, Yamada T (2011) Biocontrol of Ralstonia solanacearum by treatment with lytic bacteriophages. Appl Env Microbiol 77:4155–4162
62. Funatsu T, Taniyama T, Tajima T, Tadakuma H, Namiki H (2002) Rapid and sensitive detection method of a bacterium by using a GFP reporter phage. Microbiol Immun 46:365–369
63. Gao C, Hong M, Geng J, Zhou H, Dong J (2015) Characterization of PI (breast cancer cell special peptide) in MDA-MB-231 breast cancer cells and its potential therapeutic applications. Int J Oncol 47:1371–1378
64. Glud RN, Middleboe M (2004) Virus and bacteria dynamics of coastal sediment: implication for benthic carbon cycling. Limnol Oceanogr 49:2073–2081
65. Golkar Z, Bagasra O, Jamil N (2013) Experimental phage therapy on multiple drug resistant Pseudomonas Aeruginosa infection in mice. J Antivir Antiretrovir:S10–005. doi:10.4172/jaa.S10-005
66. Gomez P, Buckling A (2013) Coevolution with phages does not influence the evolution of bacterial mutation rates in soil. ISME J 7:2242–2244
67. Goode D, Allen VM, Barrow PA (2003) Reduction of experimental salmonella and campylobacter contamination of chicken skin by application of lytic bacteriophages. Appl Environ Microbiol 69:5032–5036
68. Goyal SM, Gerba CP, Bitton G (1987) Phage ecology. Wiley, New York, p. 321
69. Goyal SM, Zerda KS, Gerba CP (1980) Concentration of coliphages from large volumes of water and wastewater. Appl Environ Microbiol 39:85–91
70. Grabow WOK (2001) Bacteriophages: update on application as models for viruses in water. Water SA 27:251–268
71. Grabow WOK (1990) Microbiology of drinking water treatment: reclaimed wastewater. In: McFeters GA (ed) Drinking water microbiology-progress and recent developments. Springer Verlag, New York, pp. 185–203
72. Grabow WOK, Burger JS, Nupen EM (1980) Evaluation of acid-fast bacteria, Candida albicans, enteric viruses and conventional indicators for monitoring wastewater reclamation systems. Prog Water Technol 12:803–817
73. Grabow WOK, Holtzhausen CS and De Villiers JC (1993) Research on Bacteriophages as Indicators of Water Quality. WRC Report No 321/1/93 Water Res Comm Pretoria 147
74. Grabow WOK, Neubrech TE, Holtzhausen CS, Jofre J (1995) Bacteroides fragilis And Escherichia coli bacteriophages: excretion by humans and animals. Water Sci Technol 31:223–230
75. Grabow WOK, Taylor MB, Clay CG and De Villiers JC (2000) Molecular detection of viruses in drinking water: Implications for safety and disinfection. Proc. 2nd Conf. of the Int. Life Sciences Inst.: The Safety of Water Disinfection: Balancing Chem. and Microb. Risks. Radisson Deauville Resort, Miami Beach, Florida, USA, pp 15–17
76. Grabow WOK, Vrey A, Uys M and De Villiers JC (1998) Evaluation of the application of bacteriophages as indicators of water quality. WRC Report No 540/1/98. Water Res. Commission, Pretoria, p 55
77. Guenther S, Huwyler D, Richard S, Loessner MJ (2009) Virulent bacteriophage for efficient biocontrol of listeria Listeria monocytogenes in ready-to-eat foods. Appl Environ Microbiol 75:93–100
78. Haft DH, Selengut J, Mongodin EF, Nelson KE (2005) A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLoS Comput Biol 1:474–483
79. Hagens S, Habe A, Ahsen UV, Gabain A, Blasi U (2004) Therapy of experimental pseudomonas infections with a non replicating genetically modified phage Antimicrob. Agents Chemother 48:3817–3822. doi:10.1128/AAC0066-4804/04/$08.000
80. Haguenau F, Hawkes PW, Hutchison JL, Satiat-Jeunemaître B, Simon GT, Williams DB (2003) Key events in the history of the electron microscope. Microsc Microanal 9:96–138. doi:10.1017/S1431927603030113
81. Hankin EHL (1896) Action bactericide des Eaux de la Jumna et du Gange sur le vibrion du cholera. Annales de l’Institut Pasteur 10:511
82. Hanlon GW (2007) Bacteriophages: an appraisal of their role in the treatment of bacterial infections. Int J Antimicrob Agents 30:118–128
83. Ackermann HW (2011b) The first phage electron micrographs. Bacteriophage. 1(4):225–227
84. Haq IU, Chaudhry WN, Akhtar MN, Andleeb S, Qadri I (2012) Bacteriophages and their implications on future biotechnology: a review. Virol J 9:1–8
85. Haramoto E, Fujino S, Otagiri M (2015) Distinct behaviors of infectious F-specific RNA coliphage genogroups at a wastewater treatment plant. Sci Total Environ 1:32–38
86. Hart SL, Knight AM, Harbottle RP, Mistry A, Hunger HD, Cutler DF, Williamson R, Coutelle C (1994) Cell binding and internalization by filamentous phage; displaying a cyclic Arg-Gly-asp-containing peptide. The J Biol Chem 269:12468–12474
87. Havelaar AH, Hogeboom WM (1984) A method for the enumeration of male-specific bacteriophages in sewage. J Appl Bacteriol 56:439–447
88. Havelaar AH, Hogeboom WM, Pot R (1984) F-specific RNA bacteriophages in sewage; methodology and occurence. Water Sci Technol 17:645–655
89. Hayes W (1968) The genetics of bacteria and their viruses, 2nd edn. Blackwell Scientific Publications, Oxford
90. Hendrix RW (2002) Bacteriophages: evolution of the majority. Theor Popul Biol 61:471–480
91. Higgins J, Higgins S, Guenther KL, Huff W, Donoghue MA, Donoghue DJ, Hargis BM (2005) Use of specific bacteriophage treatment to reduce salmonella in poultry products. Poult Sci 84:1141–1145
92. Higuera G, Bastías R, Tsertsvadze G, Romero J, Espejo RT (2013) Recently discovered Vibrio anguillarum phages can protect against experimentally induced vibriosis in Atlantic salmon, Salmo salar. Aquaculture 392–395:128–133
93. Huff WE, Huff GR, Rath NC, Balog JM, Donoghue AM (2005) Alternatives to antibiotics: utilization of bacteriophage to treat colibacillosis and prevent foodborne pathogens. Poult Sci 84:655–659
94. Hurst CJ, McClellan KA, Benton WH (1988) Comparison of cytopathogenicity, immunofluorescence and in situ DNA hybridization as methods for the detection of adenoviruses. Water Res 22:1547–1552
95. Hwang I (2014) Virus outbreaks in chemical and biological sensors. Sensors 14(8):13592–13612. doi:10.3390/s140813592
96. Hyman P, Abedon ST (2010) Bacteriophage host range and bacterial resistance. Adv Appl Microbiol 70:217–248
97. Ignazitto G, Volterra L, Aulicino FA, D’angelo AM (1980) Coliphages as indicators in a treatment plant. Water Air Soil Pollut 13:391–398
98. Imbeault S, Parent S, Lagacé M, Uhland CF, Blais JF (2006) Using bacteriophages to prevent furunculosis caused by Aeromonas salmonicida in farmed brook trout. J Aquat Anim Health 18:203–214
99. Inal JM (2003) Phage therapy: a reappraisal of Bacteriophages as antibiotics. Archivum Immunologiae et Therapie Experimentalis 53:237–244
100. Irving LG, Smith FA (1981) One-year survey of enteroviruses, adenoviruses, and reoviruses isolated from effluent at an activated-sludge purification plant. Appl Environ Microbiol 41:51–59
101. Ishino Y, Shinagawa H, Makino K, Amemura M, Nakata A (1987) Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J Bacteriol 169:5429–5433
102. Jado I, Lopez R, Garcia E, Fenoll A, Casal J, Garcia P (2003) Phage lytic enzymes as therapy for antibiotic-resistant Streptococcus pneumoniae infection in a murine sepsis model. J Antimicrob Chemother 52:967–973
103. Jamalludeen N, She YM, Lingohr EJ, Griffiths M (2009) Isolation and characterization of virulent bacteriophages against Escherichia coli serogroups O1, O2, and O78. Poult Sci 88:1694–1702
104. Jones JB, Vallad GE, Iriarte FB, Obradović A, Wernsing MH, Jackson LE, Balogh B, Hong JC, Momo MT (2014) Considerations for using bacteriophages for plant disease control. Bacteriophage 2:208–214
105. Kamiko N, Ohgaki S (1993) Multiplication characteristics of FRNA phage and its utility as an indicator for pathogenic viruses. Water Sci Technol 27:133–136
106. Karlsson F, Borrebaeck C, Nilsson N, Malmborg-Hager AC (2003) The mechanism of bacterial infection by filamentous phages involves molecular interactions between TolA and phage protein 3 domains. J Bacteriol 8:2628–2634
107. Karunasagar I, Shivu MM, Girisha SK, Krohne G, Karunasagar I (2007) Biocontrol of pathogens in shrimp hatcheries using bacteriophages. Aquaculture 268:288–292
108. Keen EC (2012) Paradigms of pathogenesis: targeting the mobile genetic elements of disease. Front Cell Infect Microbiol 2:1–3
109. Kelly P, Anand P, Uvaydov A, Chakravartula S, Sherpa C, Pires E, O’Neil A, Douglas T, Holford M (2015) Developing a dissociative Nanocontainer for peptide drug delivery. Int J Environ Res Public Health 12:12543–12555
110. Kirsch J, Siltanen C, Zhou Q, Revzin A, Simonian A (2013) Biosensor technology: recent advances in threat agent detection and medicine. Chem Soc Reviews 42:8733–8768
111. Kodikara CP, Crew HH, Stewart GS (1991) Near on-line detection of enteric bacteria using lux recombinant bacteriophage. FEMS Microbiol Lett 67:261–265
112. Krikelis V, Markoulatos P, Spyrou N, Serie C (1985a) Detection of indigenous enteric viruses in raw sewage effluents of the city of Athens, Greece, during a two-year survey. Water Sci Technol 17:159–164
113. Krikelis V, Spyrou N, Markoulatos P, Serie C (1985b) Seasonal distribution of enteroviruses in domestic sewage. Can J Microbiol 31:24–25
114. Kruger DH, Barcak GJ, Smith HO (1988) Abolition of DNA recognition site resistance to the restriction endonuclease EcoRII. Biomed Biochim Acta 47:K1–K5
115. Krupovic M, Dutilh BE, Adriaenssens EM, Wittmann J, Vogensen FK, Sullivan MB, Rumnieks J, Prangishvili D, Lavigne R, Kropinski AM, Klumpp J, Gillis A, Enault F, Edwards RA, Duffy S, Clokie MR, Barylski J, Ackermann HW, Kuhn JH (2016) Taxonomy of prokaryotic viruses: update from the ICTV bacterial and archaeal viruses subcommittee. Arch Virol. doi:10.1007/s00705-015-2728-0
116. Kumari S, Harjai K, Chhibber S (2011) Bacteriophage versus antimicrobial agents for the treatment of murine burn wound infection caused by Klebsiella pneumoniae B5055. J Med Microbiol 60:205–210
117. Laanto E, Sundberg LR, Bamford JKH (2011) Phage specificity of the freshwater fish pathogen Flavobacterium columnare. Appl Environ Microbiol 77:7868–7872
118. Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8:317–327
119. Lakshmanan RS, Guntupalli R, Hu J, Kim DJ, Petrenko VA, Barbaree JM, Chin BA (2007) Phage immobilized magnetoelastic sensor for the detection of salmonella typhimurium. J Microbiol Meth 71:55–60
120. Lang JM, Gent DH, Schwartz HF (2007) Management of Xanthomonas leaf blight of onion with bacteriophages and a plant activator. Plant Dis 91:871–878
121. Le Romancer M, Gaillard M, Geslin C, Prieur D (2007) Viruses in extreme environments. Reviews in Environ Sci Biotech 6:17–31
122. Lee CY, Kim SJ, Park BC, Han JH (2016) Effects of dietary supplementation of bacteriophages against enterotoxigenic Escherichia coli (ETEC) K88 on clinical symptoms of post-weaning pigs challenged with the ETEC pathogen. J Anim Physiol Anim Nutr (Berl). doi:10.1111/jpn.12513
123. Leiman PG, Kanamaru S, Mesyanzhinov VV, Arisaka F, Rossmann MG (2003) Structure and morphogenesis of bacteriophage T4. Cell Mole Life Sci 60:2356–2370
124. León M, Bastías R (2015) Virulence reduction in bacteriophages resistant bacteria. Front Microbiol 6:343. doi:10.3389/fmicb.2015.00343
125. Leverentz B, Conway WS, Alavidze Z, Janisiewicz WJ, Fuchs Y, Camp MJ, Chighladze E, Sulakvelidze A (2001) Examination of bacteriophage as a biocontrol method for salmonella on fresh-cut fruit: a model study. J Food Protect 64:1116–1121
126. Li W, Caberoy NB (2010) New perspective for phage display as an efficient and versatile technology of functional proteomics. Appl Microbiol Biotechnol 85:909–919
127. Lin L, Honh W, Ji X, Han J, Huang L, Wei Y (2010) Isolation and characterization of an extremely long tail Thermus bacteriophage from Tegchong hot springs in China. J Basic Micro 50:452–456
128. Liu Y, Zhang Q, Fang C, Zhu S, Tang Y, Huang S (2005) Effect of glutathione on UV induction in prophage lambda. Arch Microbiol 183:444–449
129. Lone A, Anany H, Hakeem M, Aguis L, Avdjian AC, Bouget M, Atashi A, Brovko L, Rochefort D, Griffiths MW (2016) Development of prototypes of bioactive packaging materials based on immobilized bacteriophages for control of growth of bacterial pathogens in foods. Int J Food Microbiol 217:49–58
130. Luria SE, Anderson TF (1942) The identification and characterization of bacteriophages with the electron microscope. Proc Natl Acad Sci U S A 28:127–130. doi:10.1073/pnas.28.4.127
131. Madigan M, Martinko J (2006) Brock biology of microorganisms, 11th edn. Prentice Hall, USA
132. Mai V, Ukhanova M, Visone L, Abuladze T, Sulakvelidze A (2010) Bacteriophage Administration Reduces the Concentration of Listeria monocytogenes in the Gastrointestinal Tract and Its Translocation to Spleen and Liver in Experimentally Infected Mice. Int J Microbiol 2010:624234. doi:10.1155/2010/624234
133. Makarova KS, Grishin NV, Shabalina SA, Wolf YI, Koonin EV (2006) A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol Direct 1:7
134. Maranger R, Bird DF (1995) Viral abundance in aquatic systems: a comparison between marine and fresh waters. Mar Ecol Prog Ser 121:217–226
135. Marcó MB, Moineau S, Quiberoni A (2012) Bacteriophages and dairy fermentations. Bacteriophage. 2:149–158
136. Markoishvili K, Tsitlanadze G, Katsarava R, Morris G, Sulakvelidze A (2002) A novel sustained-release matrix based on biodegradable poly (esteramide)s and impregnated with bacteriophages and an antibiotic shows promise in management of infected venous stasis ulcers and other poorly healing wounds. Int J Dermatol 41:453–458
137. Marraffini LA (2015) CRISPR-cas immunity in prokaryotes. Nature 526:55–61
138. Marraffini LA, Sontheimer EJ (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322:1843–1845
139. Martínez-Díaz SF, Hipólito-Morales A (2013) Efficacy of phage therapy to prevent mortality during the vibriosis of brine shrimp. Aquaculture 400:120–124
140. Marza JA, Soothill JS, Boydell P, Collyns TA (2006) Multiplication of therapeutically administered bacteriophages in pseudomonas infected patients. Burns 32:644–666
141. Maszewska A, Wójcik E, Ciurzyńska A, Wojtasik A, Piątkowska I, Dastych J, Różalski A (2016) Differentiation of polyvalent bacteriophages specific to uropathogenic Proteus Mirabilis strains based on the host range pattern and RFLP. Acta Biochim Pol. doi:10.18388/abp.2015_1114
142. Mathur MD, Vidhani S, Mehndiratta PL (2003) Bacteriophage therapy: an alternative to conventional antibiotics. J Assoc Physicians India 51:593–596
143. Matsuzaki S, Yasuda M, Nishikawa H, Kuroda M, Ujihara T, Shuin T, Shen Y, Jin Z, Fujimoto S, Nasimuzzaman MÂD, Wakiguchi H, Sugihara S, Sugiura T, Koda S, Muraoka A, Imai S (2003) Experimental protection of mice against lethal Staphylococcus aureus infection by novel bacteriophage phi MR11. J Infect Dis 187:613–624
144. Mayer G (2016) Downloaded from: http://www.microbiologybook.org/mayer/phage.htm
145. McKenna F, Tarabily KAE, Hardy GESTJ, Dell B (2001) Novel in vivo use of a polyvalent Streptomyces phage to disinfest Streptomyces scabies-infected seed potatoes. Plant Pathol 50:666–675
146. Meaden S, Koskella B (2013) Exploring the risks of phage application in the environment. Front Microbiol 4:8
147. Merabishvili M, Pirnay JP, Verbeken G, Chanishvili N, Tediashvili M, Lashkhi N, Glonti T, Krylov V, Mast J, Parys LV, Lavigne R, Volckaert G, Mattheus W, Verween G, Corte PD, Rose T, Jennes S, Zizi M, Vos DD, Vaneechoutte M (2009) Quality-controlled small-scale production of a well-defined Bacteriophage cocktail for use in human clinical trials. PLoS One 4:1–104. doi:10.1371/journal.pone.0004944e4944
148. Micallef SA, Goldstein RE, George A, Ewing L, Tall BD, Boyer MS, Joseph SW, Sapkota AR (2013) Diversity, distribution and antibiotic resistance of Enterococcus spp. recovered from tomatoes, leaves, water and soil on U.S. mid-Atlantic farms. Food Microbiol 36:465–474
149. Mojica FJM, Diez-Villasenor C, Garcia-Martinez J, Soria E (2005) Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol 60:174–182
150. Mulani MS, Azhar S, Azharuddin S, Tambe S (2015) Harnessing the power of bacteriophage for pathogenreduction in wastewater. Int J Curr Microbiol Appl Sci 2:152–161
151. Murphy FA, Fauquet CM, Bishop DHL, Ghabrial SA, Jarvis AW, Martelli GP, Mayo MA, Summers MD (eds) (1995) Virus taxonomy. Sixth report of the International Committee on Taxonomy of Viruses. Springer-Verlag, New York, N.Y
152. Nagel B, Dellweg H, Gierasch LM (1992) Glossary for chemists of terms used in biotechnology—(IUPAC recommendations 1992. Pure Appl Chem 64:143–168)
153. Naidoo R, Singh A, Arya SK, Beadle B, Glass N, Tanha J, Szymanski CM, Evoy S (2012) Surface-immobilization of chromatographically purified bacteriophages for the optimized capture of bacteria. Bacteriophage 2:15–24
154. Nakai T, Park SC (2002) Bacteriophage therapy of infectious diseases in aquaculture. Res Microbiol 153:13–18
155. Nilsson AS (2014) Phage therapy--constraints and possibilities. J Med Sci 119:192–198
156. Noorlis A, Ghazali FM, Cheah YK, Tuan Zainazor TC, Ponniah J et al (2011) Prevalence and quantification of Vibrio species and Vibrio parahaemolyticus in freshwater fish at hypermarket level. Int Food Res J 18:689–695
157. Örmälä AM, Jalasvuori M (2013) Phage therapy: should bacterial resistance to phages be a concern, even in the long run? Bacteriophage 3:e24219. doi:10.4161/bact.24219
158. Otte ML, Jacob DL (2006) Constructed wetlands for phytoremediation: rhizofiltration, phytostabilisation and phytoextraction. In: Mackova M, Dowling D, Macek T (eds) Phytoremediation Rhizoremediation. Springer, Dordrecht, pp. 57–67
159. Pal C, Macia MD, Oliver A, Schachar I, Buckling A (2007) Coevolution with viruses drives the evolution of bacterial mutation rates. Nature 450:1079–1081
160. Pande J, Szewczyk MM, Grover AK (2010) Phage display: concept, innovations, applications and future. Biotechnol Adv 28:849–858
161. Park S, Nakai T (2003) Bacteriophage control of pseudomonas plecogl ossicida infection in ayu Plecoglossus altivelis. Dis Aquat Org 53:33–39
162. Park SC, Shimamura I, Fukunaga M, Mori KI, Nakai T (2000) Isolation of bacteriophages specific to a fish pathogen pseudomonas plecoglossicida as a candidate for disease control. Appl Environ Microbiol 66:1416–1422
163. Parracho HMRT, Burrowes BH, Enright MC, McConville ML, Harper DR (2012) The role of regulated clinical trials in the development of bacteriophage therapeutics. Journal of Molecular and Genetic Medicine 6:279–286
164. Paschke M (2006) Phage display systems and their applications. Appl Microbiol Biotechnol 70:2–11
165. Peltomaa R, Perolio IL, Benito-Peña E, Barderas R, Moreno-Bondi MC (2015) Application of bacteriophages in sensor development. Anal Bioanal Chem 1–24
166. Petrenko V (2008) Evolution of phage display: from bioactive peptides to bioselective nanomaterials. Expert Opin Drug Deliv 5:825–836
167. Pfankuch E, Kausche GA (1940) Isolierung und übermikroskopische Abbildung eines Bakteriophagen. Naturwissenschaften 28:46. doi:10.1007/BF01486932
168. Pietilä MK, Roine E, Sencilo A, Bamford DH, Oksanen HM (2016) Pleolipoviridae, a newly proposed family comprising archaeal pleomorphic viruses with single-stranded or double-stranded DNA genomes. Arch Virol 161(1):249–256. doi:10.1007/s00705-015-2613-x
169. Pourcel C, Salvignol G, Vergnaud G (2005) CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 151:653–663
170. Borah PK, Jindal JK, Verma JP (2000) Integrated management of bacterial leaf spot of mungbean with bacteriophages of Xav and chemicals. J Mycol Plant Pathol 30:19–21
171. Pleška M, Qian L, Okura R, Bergmiller T, Wakamoto Y, Kussell E, Guet CC (2016) Bacterial autoimmunity due to a restriction-modification system. Curr Biol 26:404–409
172. Popowska M, Rzeczycka M, Miernik A, Krawczyk-Balska A, Walsh F, Duffy B (2012) Influence of soil use on prevalence of tetracycline, streptomycin, and erythromycin resistance and associated resistance genes. Antimicrob Agents Chemother 56:1434–1443
173. Prebus A, Hillier J (1939) The construction of a magnetic electron microscope of high resolving power. Can J Res 17:49–65. doi:10.1139/cjr39a-004
174. Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen PS et al (2012) Staphylococcus aureus CC398: host adaptation and emergence of Methicillin resistance in livestock. MBio 3:00305–00311
175. Prigent M, Leroy M, Confalonieri F, Dutertre M, DuBow MS (2005) A diversity of bacteriophages forms and genomes can be isolated from the surface sands of Sahara Desert. Extremophiles 9:289–296
176. Ptashne M (2006) Lambda’s switch: lessons from a modules wap. Curr Biol 16:459–462
177. Quintin F, Kerrigan WC, Soothill JS (2005) Experimental bacteriophage protection against Staphylococcus aureus abscesses in a rabbit model. Antimicrob Agents Chemother 1220–1221
178. Rackus DG, Shamsi MH, Wheeler AR (2015) Electrochemistry, biosensors and microfluidics: a convergence of fields. Chem Soc Rev 44:5320–5340
179. Rahmani R, Zarrini G, Sheikhzadeh F, Zadeh NAM (2015) Effective phages as green antimicrobial agents against antibiotic-resistant hospital Escherichia coli jundishapur. J Microbiol 8(2):e17744
180. Rakhuba DV, Kolomiets EI, Dey ES, Novik GI (2010) Bacteriophage receptors, mechanisms of phage adsorption and penetrationinto host cell. Pol J Microbiol 59:145–155
181. Ravat F, Jault P, Gabard J (2015) Bactériophages et phagothérapie: utilisation de virus Naturels pour traiter les infections bactériennes. Ann Burns Fire Disasters 28:13–20
182. Ravensdale M, Blom TJ, Garza JAG, Svircev AM, Smith RJ (2007) Bacteriophages and the control of Erwinia carotovora subsp. Carotovora Can J Plant Pathol 29:121–130
183. Reardon S (2014) Phage therapy gets revitalized. Nature 510:15–16
184. Rhoads DD, Wolcott RD, Kuskowski MA, Wolcott BM, Ward LS, Sulakvelidze A (2009) Bacteriophage therapy of venous leg ulcers in humans: results of a phase I safety trial. J Wound Care 18:237–243
185. Rivas L, Coffey B, McAuliffe O, Coffey A, Ross RP, McDonnell MJ, Duffy G, Burgess CM (2010) In vivo and ex vivo evaluations of Bacteriophages e11/2 and e4/1c for use in the control of Escherichia coli O157:H7. Appl Environ Microbiol 76:7210–7216
186. Ruska H (1940) Über die Sichtbarmachung der bakteriophagen Lyse im Übermikroskop. Naturwissenschaften 28:45–46. doi:10.1007/BF01486931
187. Saksida S, Constantine J, Karreman GA, Neville C, Sweeting R, Beamish R (2006) Evaluation of sea lice, Lepeophtheirus salmonis, abundance levels on farmed salmon in British Columbia, Canada. In The Proceedings from the International Symposium 6–11 august on Veterinary Epidemiology and Economics XI, Cairns, Australia
188. Sangster W, Hegarty JP, Stewart DB (2014) Phage therapy for Clostridium difficile infection: an alternative to antibiotics? Seminars in Colon and Rectal Surgery 25(3):167–170
189. Sangster W, Hegarty JP, Stewart DB Sr (2015) Phage tail-like particles kill Clostridium Difficile and represent an alternative to conventional antibiotics. Surgery 157:96–103
190. Sarker SA, McCallin S, Barretto C, Berger B, Pittet AC, Sultana S, Krause L, Huq S, Bibiloni R, Bruttin A, Reuteler G, Brussow H (2012) Oral T4-like phage cocktail application to healthy adult volunteers from Bangladesh. Virology 434:222–232
191. Säwström CH, Lisle J, Anesio AM, Priscu JC, Laybourn-Parry J (2008) Bacteriophage in polar inland waters. Extremophiles 12:167–175
192. Servick K (2016) Beleaguered phage therapy trial presses on. Science 352:1506
193. Sharma M, Patel JR, Conway WS, Ferquson S, Sulakvelidze A (2009) Effectiveness of bacteriophage in reducing Escherichia coli o157:H7 on fresh cut cantaloupes and lettuce. J Food Protect 72:1481–1485
194. Sidhu SS (2000) Phage display in pharmaceutical biotechnology. Curr Opin Chem Biol 11:610–616
195. Silva YJ, Costa L, Pereira C, Mateus C, Cunha Â, Calado R, Gomes NCM, Pardo MA, Hernandez I, Almeida A (2014) Phage therapy as an approach to prevent Vibrio anguillarum infections in fish larvae production. PLoS One 9:e114197. doi:10.1371/journal.pone.0114197
196. Singh A, Arya SK, Glass N, Hanifi-Moghaddam P, Naidoo R, Szymanski CM, Tanha J, Evoy S (2010) Bacteriophage tail spike proteins as molecular probes for sensitive and selective bacterial detection. Biosens Bioelectron 26:131–138
197. Singh A, Poshtiban S, Evoy S (2013) Recent advances in Bacteriophage based biosensors for food-borne pathogen detection. Sensors 13:1763–1786. doi:10.3390/s130201763
198. Smith GP (1985) Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228:1315–1317
199. Sperinde JJ, Choi SJ, Szoka FC Jr (2001) Phage display selection of a peptide DNaseII inhibitor that enhances gene delivery. The Journal of Gene Medicine 3:101–108
200. Stewart GSAB, Smith T, Denyer S (1989) Genetic engineering for bioluminescent bacteria. Food Sci and Tech Today 3:19–22
201. Subasinghe RP, Bondad-Reantaso MG, McGladdery SE (2001) Aquaculture development, health and wealth. In Aquaculture in the Millennium. Technica l Proceedings of the Conference on Aquaculture in the Third Millennium; Suba singhe RP, Bueno P, Phillips MJ, Hough C, McGladdery SE, Arthur JR, Eds Bangkok Thailand
202. Sulakvelidze A, Alavidze Z, Morris JG Jr (2001) Bacteriophage therapy. Antimicrob Agents Chemother 45:649–659
203. Sulakvelidze A, Kutter E (2005) Bacteriophage therapy in humans. In: Kutter E, Sulakvelidze A (eds) Bacteriophages: biology and applications. CRC Press, USA, pp. 381–436
204. Summers WC (1999) Felix d’Herelle and the origins of molecular biology. Yale University Press, New Haven, Conn
205. Suttle CA (2005) Viruses in the sea. Nature 437:356–361
206. Suttle CA (2007) Marine viruses - major players in the global ecosystem. Nat Rev Microbiol 5:801–812
207. Sybesma W, Zbinden R, Chanishvili N, Kutateladze M, Chkhotua A, Ujmajuridze A, Mehnert U, Kessler TM (2016) Bacteriophages as potential treatment for urinary tract infections. Front Microbiol 7:465. doi:10.3389/fmicb.2016.00465
208. Tan D, Gram L, Middelboe M (2014) Vibriophages and their interactions with the fish pathogen Vibrio anguillarum. Appl Environ Microbiol 80:3128–3140
209. Tartera C, Lucena F, Jofre J (1989) Human origin of Bacteroides fragilis bacteriophages present in the environment. Appl Environ Microbiol 55:2696–2701
210. Thompson CC, Amaral GR, Campeão M, Edwards RA, Polz MF, Dutilh BE, Ussery DW, Sawabe T, Swings J (2015) Microbial taxonomy in the post-genomic era: rebuilding from scratch? Archiv Microbiol 197:359–370
211. Tock MR, Dryden DT (2005) The biology of restriction and anti-restriction. Curr Opin Microbiol 8:466–472
212. Toro H, Price SB, McKee AS, Hoerr FJ, Krehling J, Perdue M, Bauermeister L (2005) Use of bacteriophages in combination with competitive exclusion to reduce salmonella from infected chickens. Avian Dis 9:118–124
213. Twort FW (1915) An investigation on the nature of ultra-microscopic viruses. Lancet 2:1241–1243
214. Twort FW (1922) The bacteriophage: the breaking down of bacteria by associated filter passing lysins. Br Med J 2:293–296
215. Twort FW (1949) The discovery of the bacteriophage. Science News 14:33–34
216. Van Helvoort T (1992) Bacteriological and physiological research styles in the early controversy on the nature of the bacteriophage phenomenon. Med Hist 3:243–270
217. Verner-Jeffreys DW, Algoet M, Pond MJ, Virdee HK, Bagwell NJ, Roberts EG (2007) Furunculosis in Atlantic salmon (Salmo salar L.) is not readily controllable by bacteriophage therapy. Aquaculture 270:475–484
218. Viertel TM, Ritter K, Horz HP (2014) Viruses versus bacteria-novel approaches to phage therapy as a tool against multidrug-resistant pathogens. J Antimicrob Chemother 69:2326–2336
219. Vinod MG, Shivu MM, Umesha KR, Rajeeva BC, Krohne G, Indrani K, Iddya K (2006) Isolation of Vibrio harveyi bacteriophage with a potential for biocontrol of luminous vibriosis in hatchery environments. Aquaculture 255:117–124
220. Wagner P, Acheson D, Waldor M (2001) Human neutrophils and their products induce Shiga toxin production by enterohemorrhagic Escherichiacoli. Infect Immun 69:1934–1937
221. Wang Z, Wang D, Chen J, Sela DA, Nugen SR (2016) Development of a novel bacteriophage based biomagnetic separation method as an aid for sensitive detection of viable Escherichia coli. Analyst 141:1009–1016
222. Watanabe R, Matsumoto T, Sano G, Ishii Y, Tateda K, Sumiyama Y, Uchiyama J, Sakurai S, Matsuzaki S, Imai S, Yamaguchi K (2007) Efficacy of bacteriophage therapy against gut-derived sepsis caused by Pseudomonas aeruginosa in mice. Antimicrob Agents Che mother 51:446–452
223. Watson BB, Eveland WC (1965) The application of the phage fluorescent antiphage staining system in the specific identification of Listeria monocytogenes. I. Species specificity and immunofluorescent sensitivity of Listeria monocytogenes phage observed in smear preparations. Journal of Infectious Disease 115:363–369
224. Weitz JS, Wilhelm SW (2012) Ocean viruses and their effects on microbial communities and biogeochemical cycles. F1000 Biology Reports 4:17. doi:10.3410/B4-17
225. Weitz JS and Wilhelm SW (2013) An ocean of viruses. The Scientist (July 1st issue). http://www.the-scientist.com/?articles.view/articleNo/36120/title/An-Ocean-of-Viruses/. Downloaded 3 Jan 2016
226. Wicki M, Auckenthaler A, Felleisen R, Karabulut F, Niederhauser I, Tanner M, Baumgartner A (2015) Assessment of source tracking methods for application in spring water. J Water Health 13:473–488
227. Wildy P (1971) Classification and nomenclature of viruses. First report of the International Committee on Nomenclature of Viruses. S. Karger, Basel
228. Willats WG (2002) Phage display: practicalities and prospects. Plant Mol Biol 50:837–854
229. Williamson KE, Radosevich M, Wommack KE (2005) Abundance and diversity of viruses in six Delaware soils. Appl Environ Microbiol 71:3119–3125
230. Williamson KE, Wommack KE, Radosevich M (2003) Sampling natural viral communities from soil for culture-independent analyses. Appl Environ Microbiol 69:6628–6633
231. Wills QF, Kerrigan C, Soothill JS (2005) Experimental bacteriophage protection against Staphylococcus aureus abscesses in a rabbit model. Antimicrob Agents Chemother 49:1220–1221
232. Withey S, Cartmell E, Avery LM, Stephenson T (2005) Bacteriophages—potential for application in wastewater treatment processes. Sci Total Environ 339:1–18
233. Wlodarczyk KD, Vandenheuve D, Jang HB, Olszak T, Arabski M, Wasik S, Drabik M, Briers Y, Higgins G, Tyrrell J, Harvey BJ, Noben JP, Lavigne R, Kawa ZD (2016) A proposed integrated approach for the preclinical evaluation of phage therapy in pseudomonas infections (2016). Scientific RepoRts 6:28115. doi:10.1038/srep28115
234. Wright A, Hawkins CH, Anggård EE, Harper DR (2009a) A controlled clinical trial of a therapeutic bacteriophage preparation in chronic otitis due to antibiotic-resistant Pseudomonas aeruginosa; a preliminary report of efficacy. Clin Otolaryngol 34:349–357
235. Young R, Wang IN, Roof WD (2000) Phages will out: strategies of host cell lysis. Trends Microbiol 8:120–128
236. Zhu YG, Johnson TA, Su JQ, QiaoM GGX, Stedtfeld RD et al (2013) Diverse and abundant antibiotic resistance genes in Chineses wine farms. Proceedings of the National Academy of Sciences USA 110:3435–3440
237. Zschach H, Joensen KG, Lindhard B, Lund O, Goderdzishvili M, Chkonia I, Jgenti G, Kvatadze N, Alavidze Z, Kutter EM, Hasman H, Larsen MV (2015) What can we learn from a metagenomic analysis of a Georgian Bacteriophage cocktail? Viruses 7:6570–6589