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Bacteriophages and its applications: an overview

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Abstract

Bacteriophages (or phages), the most abundant viral entity of the planet, are omni-present in all the ecosystems. On the basis of their unique characteristics and anti-bacterial property, phages are being freshly evaluated taxonomically. Phages replicate inside the host either by lytic or lysogenic mode after infecting and using the cellular machinery of a bacterium. Since their discovery by Twort and d’Herelle in the early 1900s, phage became an important agent for combating pathogenic bacteria in clinical treatments and its related research gained momentum. However, due to recent emergence of bacterial resistance on antibiotics, applications of phage (phage therapy) become an inevitable option of research. Phage particles become popular as a biotechnological tool and treatment of pathogenic bacteria in a range of applied areas. However, there are few concerns over the application of phage-based solutions. This review deals with the updated phage taxonomy (ICTV 2015 Release and subsequent revision) and phage biology and the recent development of its application in the areas of biotechnology, biosensor, therapeutic medicine, food preservation, aquaculture diseases, pollution remediation, and wastewater treatment and issues related with limitations of phage-based remedy.

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References

  • Abedon ST (2016) Bacteriophage exploitation of bacterial biofilms: phage preference for less mature targets? FEMS Microbiol Lett. doi:10.1093/femsle/fnv246

    Google Scholar 

  • Abedon ST, Herschler TD, Stopar D (2001) Bacteriophage latent-period evolution as a response to resource availability. Appl Environ Microbiol 13:4233–4241

    Article  Google Scholar 

  • Abedon ST, Sarah JK, Bob GB, Kutter EM (2011) Phage treatment of human infections. Bacteriophage. 1(2):66–85

    Article  PubMed  PubMed Central  Google Scholar 

  • Abeles AL, Snyder KM, Chattoraj DK (1984) P1 plasmid replication: replicon structure. J Mol Biol 17:307–324

    Article  Google Scholar 

  • Ackermann HW (2011a) Bacteriophage taxonomy Microbiology Australia, 90–94. Downloaded from http://journals.cambridgemedia.com.au/UserDir/CambridgeJournal/Articles/11%20ackermann244.pdf

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alisky J, Iczkowski K, Rapoport A, Troitsky N (1998) Bacteriophages show promise as antimicrobial agents. J Infect 36:5–15

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Balogh B, Canteros BI, Stall RE, Jones JB (2008) Control of citrus canker and citrus bacterial spot with bacteriophages. Plant Dise 92:1048–1052

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bell RG (1976) The limitation of the ratio of fecal coliform to total coliphage as a water pollution index. Water Res 10:745–748

    Article  Google Scholar 

  • Benhar I (2001) Biotechnological applications of phage and cell display. Biotechnol Adv 19:1–33

    Article  CAS  PubMed  Google Scholar 

  • Bickle TA, Kruger DH (1993) Biology of DNA restriction. Microbiol Rev 57:434–450

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Borgaro JG, Zhu Z (2013) Characterization of the 5-hydroxymethylcytosine-specific DNA restriction endonucleases. Nucleic Acids Res 41:4198–4206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradley DE (1967) Ultrastructure of bacteriophages and bacteriocins. Bacteriol Rev 31:230–314

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bradley DE, Kay D (1960) The fine structure of Bacteriophages. J Gen Microbiol 23:553–563

    Article  Google Scholar 

  • Breitbart M (2012) Marine viruses: truth or dare. Annu Rev Mar Sci 4:425–448

    Article  Google Scholar 

  • Breitbart M, Wegley L, Leeds S, Schoenfeld T, Rohwer F (2004) Phage community dynamics in hot springs. Appl Environ Microbiol 70:1633–1640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Brenner S, Streisinger G, Horne RW, Champe SP, Barnett L, Benzer S, Rees MW (1959) Structural components of bacteriophage. J Mol Biol 1:281

    Article  CAS  Google Scholar 

  • Brock TD, Madigan, Michael T (1988) Biology of microorganisms, 5th edn. Prentice-Hall, USA, pp. 1988–1835

    Google Scholar 

  • 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

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruynoghe R, Maisin J (1921) Essais de theârapeutique au moyen du bacteriophage. J Soc Biol 85:1120–1121

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buckling A, Rainey PB (2002) Antagonistic coevolution between a bacterium and a bacteriophage. P Roy Soc B Biol Sci 269:931–936

    Article  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Cademartiri R, Anany H, Gross I, Bhayani R, Griffiths M, Brook MA (2010) Immobilization of bacteriophages on modified silica particles. Biomaterials 31:1904–1910

    Article  CAS  PubMed  Google Scholar 

  • Campbell NA, Reece JB (2005) Biology. Pearson, Benjamin Cummings, San Francisco, pp. 338–339

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Clark JR, March JB (2004) Bacterial viruses as human vaccines? Expert Rev Vaccines 3:463–476

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Cui Z (2015) Advances in the treatment of wound bacterial infection with phage. Zhonghua Shao Shang ZaZhi 31:389–391

    Google Scholar 

  • D’Herelle F (1917a) Sur un microbe invisible antagoniste des bacillesdysente ´riques. C R Academy of Sciences (Paris) 165:373–375

    Google Scholar 

  • D’Herelle F (1930) The bacteriophage and its clinical applications. Charles C Thomas, Springfield, Ill

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • d’Herelle F (1917b) On an invisible microbe antagonistic to dysentery bacilli. Comptes Rendus Academie des Sciences 165:373–375

    Google Scholar 

  • d’Herelle F (1949) The bacteriophage. Science News 14:44–59

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duckworth DH (1976) Who discovered Bacteriophage? Bacteriol Rev 40:793–802

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duckworth DH, Gulig PA (2002) Bacteriophages: potential treatment for bacterial infections. BioDrugs 16:57–62

    Article  CAS  PubMed  Google Scholar 

  • DuPont HL (2007) The growing threat of foodborne bacterial enteropathogens of animal origin. Clin Infect Dis 45:1353–1361

    Article  PubMed  Google Scholar 

  • FAO Report (2015) Downloaded from: http://www.fao.org/3/a-i4910e.pdf. Accessed 09 Jan 2016

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Flegel TW (2006) Detection of major penaeid shrimp viruses in Asia, a historical perspective with emphasis on Thailand. Aquaculture 258:1–33

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Glud RN, Middleboe M (2004) Virus and bacteria dynamics of coastal sediment: implication for benthic carbon cycling. Limnol Oceanogr 49:2073–2081

    Article  Google Scholar 

  • 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

  • Gomez P, Buckling A (2013) Coevolution with phages does not influence the evolution of bacterial mutation rates in soil. ISME J 7:2242–2244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goyal SM, Gerba CP, Bitton G (1987) Phage ecology. Wiley, New York, p. 321

    Google Scholar 

  • Goyal SM, Zerda KS, Gerba CP (1980) Concentration of coliphages from large volumes of water and wastewater. Appl Environ Microbiol 39:85–91

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grabow WOK (2001) Bacteriophages: update on application as models for viruses in water. Water SA 27:251–268

    Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

  • 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

  • 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

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Hanlon GW (2007) Bacteriophages: an appraisal of their role in the treatment of bacterial infections. Int J Antimicrob Agents 30:118–128

    Article  CAS  PubMed  Google Scholar 

  • Ackermann HW (2011b) The first phage electron micrographs. Bacteriophage. 1(4):225–227

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Havelaar AH, Hogeboom WM (1984) A method for the enumeration of male-specific bacteriophages in sewage. J Appl Bacteriol 56:439–447

    Article  CAS  PubMed  Google Scholar 

  • Havelaar AH, Hogeboom WM, Pot R (1984) F-specific RNA bacteriophages in sewage; methodology and occurence. Water Sci Technol 17:645–655

    Google Scholar 

  • Hayes W (1968) The genetics of bacteria and their viruses, 2nd edn. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • Hendrix RW (2002) Bacteriophages: evolution of the majority. Theor Popul Biol 61:471–480

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hwang I (2014) Virus outbreaks in chemical and biological sensors. Sensors 14(8):13592–13612. doi:10.3390/s140813592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hyman P, Abedon ST (2010) Bacteriophage host range and bacterial resistance. Adv Appl Microbiol 70:217–248

    Article  CAS  PubMed  Google Scholar 

  • Ignazitto G, Volterra L, Aulicino FA, D’angelo AM (1980) Coliphages as indicators in a treatment plant. Water Air Soil Pollut 13:391–398

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Inal JM (2003) Phage therapy: a reappraisal of Bacteriophages as antibiotics. Archivum Immunologiae et Therapie Experimentalis 53:237–244

    Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Karunasagar I, Shivu MM, Girisha SK, Krohne G, Karunasagar I (2007) Biocontrol of pathogens in shrimp hatcheries using bacteriophages. Aquaculture 268:288–292

    Article  Google Scholar 

  • Keen EC (2012) Paradigms of pathogenesis: targeting the mobile genetic elements of disease. Front Cell Infect Microbiol 2:1–3

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kodikara CP, Crew HH, Stewart GS (1991) Near on-line detection of enteric bacteria using lux recombinant bacteriophage. FEMS Microbiol Lett 67:261–265

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Krikelis V, Spyrou N, Markoulatos P, Serie C (1985b) Seasonal distribution of enteroviruses in domestic sewage. Can J Microbiol 31:24–25

    Article  CAS  PubMed  Google Scholar 

  • Kruger DH, Barcak GJ, Smith HO (1988) Abolition of DNA recognition site resistance to the restriction endonuclease EcoRII. Biomed Biochim Acta 47:K1–K5

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Laanto E, Sundberg LR, Bamford JKH (2011) Phage specificity of the freshwater fish pathogen Flavobacterium columnare. Appl Environ Microbiol 77:7868–7872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8:317–327

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Le Romancer M, Gaillard M, Geslin C, Prieur D (2007) Viruses in extreme environments. Reviews in Environ Sci Biotech 6:17–31

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Leiman PG, Kanamaru S, Mesyanzhinov VV, Arisaka F, Rossmann MG (2003) Structure and morphogenesis of bacteriophage T4. Cell Mole Life Sci 60:2356–2370

    Article  CAS  Google Scholar 

  • León M, Bastías R (2015) Virulence reduction in bacteriophages resistant bacteria. Front Microbiol 6:343. doi:10.3389/fmicb.2015.00343

    PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Madigan M, Martinko J (2006) Brock biology of microorganisms, 11th edn. Prentice Hall, USA

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maranger R, Bird DF (1995) Viral abundance in aquatic systems: a comparison between marine and fresh waters. Mar Ecol Prog Ser 121:217–226

    Article  Google Scholar 

  • Marcó MB, Moineau S, Quiberoni A (2012) Bacteriophages and dairy fermentations. Bacteriophage. 2:149–158

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Marraffini LA (2015) CRISPR-cas immunity in prokaryotes. Nature 526:55–61

    Article  CAS  PubMed  Google Scholar 

  • Marraffini LA, Sontheimer EJ (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322:1843–1845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martínez-Díaz SF, Hipólito-Morales A (2013) Efficacy of phage therapy to prevent mortality during the vibriosis of brine shrimp. Aquaculture 400:120–124

    Article  Google Scholar 

  • Marza JA, Soothill JS, Boydell P, Collyns TA (2006) Multiplication of therapeutically administered bacteriophages in pseudomonas infected patients. Burns 32:644–666

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Mathur MD, Vidhani S, Mehndiratta PL (2003) Bacteriophage therapy: an alternative to conventional antibiotics. J Assoc Physicians India 51:593–596

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Mayer G (2016) Downloaded from: http://www.microbiologybook.org/mayer/phage.htm

  • 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

    Article  Google Scholar 

  • Meaden S, Koskella B (2013) Exploring the risks of phage application in the environment. Front Microbiol 4:8

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Nagel B, Dellweg H, Gierasch LM (1992) Glossary for chemists of terms used in biotechnology—(IUPAC recommendations 1992. Pure Appl Chem 64:143–168

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Nakai T, Park SC (2002) Bacteriophage therapy of infectious diseases in aquaculture. Res Microbiol 153:13–18

    Article  PubMed  Google Scholar 

  • Nilsson AS (2014) Phage therapy--constraints and possibilities. J Med Sci 119:192–198

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Pande J, Szewczyk MM, Grover AK (2010) Phage display: concept, innovations, applications and future. Biotechnol Adv 28:849–858

    Article  CAS  PubMed  Google Scholar 

  • Park S, Nakai T (2003) Bacteriophage control of pseudomonas plecogl ossicida infection in ayu Plecoglossus altivelis. Dis Aquat Org 53:33–39

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paschke M (2006) Phage display systems and their applications. Appl Microbiol Biotechnol 70:2–11

    Article  CAS  PubMed  Google Scholar 

  • Peltomaa R, Perolio IL, Benito-Peña E, Barderas R, Moreno-Bondi MC (2015) Application of bacteriophages in sensor development. Anal Bioanal Chem 1–24

  • Petrenko V (2008) Evolution of phage display: from bioactive peptides to bioselective nanomaterials. Expert Opin Drug Deliv 5:825–836

    Article  CAS  PubMed  Google Scholar 

  • Pfankuch E, Kausche GA (1940) Isolierung und übermikroskopische Abbildung eines Bakteriophagen. Naturwissenschaften 28:46. doi:10.1007/BF01486932

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ptashne M (2006) Lambda’s switch: lessons from a modules wap. Curr Biol 16:459–462

    Article  CAS  Google Scholar 

  • Quintin F, Kerrigan WC, Soothill JS (2005) Experimental bacteriophage protection against Staphylococcus aureus abscesses in a rabbit model. Antimicrob Agents Chemother 1220–1221

  • Rackus DG, Shamsi MH, Wheeler AR (2015) Electrochemistry, biosensors and microfluidics: a convergence of fields. Chem Soc Rev 44:5320–5340

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Reardon S (2014) Phage therapy gets revitalized. Nature 510:15–16

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruska H (1940) Über die Sichtbarmachung der bakteriophagen Lyse im Übermikroskop. Naturwissenschaften 28:45–46. doi:10.1007/BF01486931

    Article  CAS  Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Säwström CH, Lisle J, Anesio AM, Priscu JC, Laybourn-Parry J (2008) Bacteriophage in polar inland waters. Extremophiles 12:167–175

    Article  PubMed  Google Scholar 

  • Servick K (2016) Beleaguered phage therapy trial presses on. Science 352:1506

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sidhu SS (2000) Phage display in pharmaceutical biotechnology. Curr Opin Chem Biol 11:610–616

    CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith GP (1985) Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228:1315–1317

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Stewart GSAB, Smith T, Denyer S (1989) Genetic engineering for bioluminescent bacteria. Food Sci and Tech Today 3:19–22

    Google Scholar 

  • 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

  • Sulakvelidze A, Alavidze Z, Morris JG Jr (2001) Bacteriophage therapy. Antimicrob Agents Chemother 45:649–659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Summers WC (1999) Felix d’Herelle and the origins of molecular biology. Yale University Press, New Haven, Conn

    Google Scholar 

  • Suttle CA (2005) Viruses in the sea. Nature 437:356–361

    Article  CAS  PubMed  Google Scholar 

  • Suttle CA (2007) Marine viruses - major players in the global ecosystem. Nat Rev Microbiol 5:801–812

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Tan D, Gram L, Middelboe M (2014) Vibriophages and their interactions with the fish pathogen Vibrio anguillarum. Appl Environ Microbiol 80:3128–3140

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tartera C, Lucena F, Jofre J (1989) Human origin of Bacteroides fragilis bacteriophages present in the environment. Appl Environ Microbiol 55:2696–2701

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Tock MR, Dryden DT (2005) The biology of restriction and anti-restriction. Curr Opin Microbiol 8:466–472

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Twort FW (1915) An investigation on the nature of ultra-microscopic viruses. Lancet 2:1241–1243

    Article  Google Scholar 

  • Twort FW (1922) The bacteriophage: the breaking down of bacteria by associated filter passing lysins. Br Med J 2:293–296

    Google Scholar 

  • Twort FW (1949) The discovery of the bacteriophage. Science News 14:33–34

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wagner P, Acheson D, Waldor M (2001) Human neutrophils and their products induce Shiga toxin production by enterohemorrhagic Escherichiacoli. Infect Immun 69:1934–1937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

  • 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

    Article  PubMed  Google Scholar 

  • Wildy P (1971) Classification and nomenclature of viruses. First report of the International Committee on Nomenclature of Viruses. S. Karger, Basel

    Google Scholar 

  • Willats WG (2002) Phage display: practicalities and prospects. Plant Mol Biol 50:837–854

    Article  CAS  PubMed  Google Scholar 

  • Williamson KE, Radosevich M, Wommack KE (2005) Abundance and diversity of viruses in six Delaware soils. Appl Environ Microbiol 71:3119–3125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williamson KE, Wommack KE, Radosevich M (2003) Sampling natural viral communities from soil for culture-independent analyses. Appl Environ Microbiol 69:6628–6633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wills QF, Kerrigan C, Soothill JS (2005) Experimental bacteriophage protection against Staphylococcus aureus abscesses in a rabbit model. Antimicrob Agents Chemother 49:1220–1221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Withey S, Cartmell E, Avery LM, Stephenson T (2005) Bacteriophages—potential for application in wastewater treatment processes. Sci Total Environ 339:1–18

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Young R, Wang IN, Roof WD (2000) Phages will out: strategies of host cell lysis. Trends Microbiol 8:120–128

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors sincerely acknowledge Professor Andrew M. Kropinski, Departments of Food Science, Molecular and Cellular Biology and Pathobiology, University of Guelph, Canada and the chair of the Bacterial and Archaeal Viruses Subcommittee, for his kind suggestion and help related to bacteriophage taxonomy. Authors also acknowledge Director, Defense Research Laboratory for his kind support. Sincere thanks are also due to Mrs. Swagata Chatterjee for her contribution in making handmade figures. Further, sincere apology is being conveyed from the authors for the many colleagues whose works could not be referred to in this manuscript due to space limitations.

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Correspondence to Soumya Chatterjee.

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Sonika Sharma and Soumya Chatterjee contributed equally.

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Sharma, S., Chatterjee, S., Datta, S. et al. Bacteriophages and its applications: an overview. Folia Microbiol 62, 17–55 (2017). https://doi.org/10.1007/s12223-016-0471-x

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