Skip to main content
SpringerLink
Log in

Biofilm control with natural and genetically-modified phages

  • REVIEW
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Bacteriophages, as the most dominant and diverse entities in the universe, have the potential to be one of the most promising therapeutic agents. The emergence of multidrug-resistant bacteria and the antibiotic crisis in the last few decades have resulted in a renewed interest in phage therapy. Furthermore, bacteriophages, with the capacity to rapidly infect and overcome bacterial resistance, have demonstrated a sustainable approach against bacterial pathogens-particularly in biofilm. Biofilm, as complex microbial communities located at interphases embedded in a matrix of bacterial extracellular polysaccharide substances (EPS), is involved in health issues such as infections associated with the use of biomaterials and chronic infections by multidrug resistant bacteria, as well as industrial issues such as biofilm formation on stainless steel surfaces in food industry and membrane biofouling in water and wastewater treatment processes. In this paper, the most recent studies on the potential of phage therapy using natural and genetically-modified lytic phages and their associated enzymes in fighting biofilm development in various fields including engineering, industry, and medical applications are reviewed. Phage-mediated prevention approaches as an indirect phage therapy strategy are also explored in this review. In addition, the limitations of these approaches and suggestions to overcome these constraints are discussed to enhance the efficiency of phage therapy process. Finally, future perspectives and directions for further research towards a better understanding of phage therapy to control biofilm are recommended.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abedon ST, Kuhl SJ, Blasdel BG, Kutter EM (2011) Phage treatment of human infections. Bacteriophage 1(2):66–85

    Article  Google Scholar 

  • Abuladze T, Li M, Menetrez MY, Dean T, Senecal A, Sulakvelidze A (2008) Bacteriophages reduce experimental contamination of hard surfaces, tomato, spinach, broccoli, and ground beef by Escherichia coli O157: H7. Appl Environ Microbiol 74(20):6230–6238

    Article  CAS  Google Scholar 

  • Alisky J, Iczkowski K, Rapoport A, Troitsky N (1998) Bacteriophages show promise as antimicrobial agents. J Infect 36(1):5–15

    Article  CAS  Google Scholar 

  • Azeredo J, Sutherland IW (2008) The use of phages for the removal of infectious biofilms. Curr Pharm Biotechnol 9(4):261–266

    Article  CAS  Google Scholar 

  • Bales PM, Renke EM, May SL, Shen Y, Nelson DC (2013) Purification and characterization of biofilm-associated EPS exopolysaccharides from ESKAPE organisms and other pathogens. PLoS ONE 8(6):e67950

    Article  CAS  Google Scholar 

  • Bedi MS, Verma V, Chhibber S (2009) Amoxicillin and specific bacteriophage can be used together for eradication of biofilm of Klebsiella pneumoniae B5055. World J Microbiol Biotechnol 25(7):1145–1151  

    Article  CAS  Google Scholar 

  • Bender KO, Garland M, Ferreyra JA, Hryckowian AJ, Child MA, Puri AW, Solow-Cordero DE, Higginbottom SK, Segal E, Banaei N, Shen A, Sonnenburg JL (2015) A small-molecule antivirulence agent for treating Clostridium difficile infection. Sci Transl Med 7(306):306ra148–306ra148

    Article  Google Scholar 

  • Bhattacharjee AS, Choi JD, Motlagh AM, Mukherji ST, Goel R (2015) Bacteriophage therapy for membrane biofouling in membrane bioreactors and antibiotic-resistant bacterial biofilms. Biotechnol Bioeng 112(8):1644–1654

    Article  CAS  Google Scholar 

  • Born Y, Fieseler L, Klumpp J, Eugster MR, Zurfluh K, Duffy B, Loessner MJ (2014) The tail-associated depolymerase of Erwinia amylovora phage L1 mediates host cell adsorption and enzymatic capsule removal, which can enhance infection by other phage. Environ Microbiol 16(7):2168–2180

    Article  CAS  Google Scholar 

  • Borysowski J, Weber-Dąbrowska B, Górski A (2006) Bacteriophage endolysins as a novel class of antibacterial agents. Exp Biol Med 231(4):366–377

    CAS  Google Scholar 

  • Brabban AD, Hite E, Callaway TR (2005) Evolution of foodborne pathogens via temperate bacteriophage-mediated gene transfer. Foodbourne Pathog Dis 2(4):287–303

    Article  CAS  Google Scholar 

  • Briandet R, Lacroix-Gueu P, Renault M, Lecart S, Meylheuc T, Bidnenko E, Fontaine-Aupart MP (2008) Fluorescence correlation spectroscopy to study diffusion and reaction of bacteriophages inside biofilms. Appl Environ Microbiol 74(7):2135–2143

    Article  CAS  Google Scholar 

  • Brockhurst MA, Buckling A, Rainey PB (2006) Spatial heterogeneity and the stability of host-parasite coexistence. J Evolut Biol 19(2):374–379

    Article  CAS  Google Scholar 

  • Bura R, Cheung M, Liao B, Finlayson J, Lee BC, Droppo IG, Liss SN (1998) Composition of extracellular polymeric substances in the activated sludge floc matrix. Water Sci Technol 37(4):325–333

    Article  CAS  Google Scholar 

  • Burrowes B, Harper DR, Anderson J, McConville M, Enright MC (2011) Bacteriophage therapy: potential uses in the control of antibiotic-resistant pathogens. Expert Rev Anti-infective Ther 9(9):775–785

    Article  Google Scholar 

  • Casjens S (2003) Prophages and bacterial genomics: what have we learned so far? Mol Microbiol 49(2):277–300

    Article  CAS  Google Scholar 

  • Chaitiemwong N, Hazeleger WC, Beumer RR (2014) Inactivation of Listeria monocytogenes by disinfectants and bacteriophages in suspension and stainless steel carrier tests. J Food Prot 77(12):2012–2020

    Article  CAS  Google Scholar 

  • Chan BK, Abedon ST (2012) 1 phage therapy pharmacology: phage cocktails. Adv Appl Microbiol 78:1

    Article  CAS  Google Scholar 

  • Chan BK, Abedon ST, Loc-Carrillo C (2013) Phage cocktails and the future of phage therapy. Future Microbiol 8(6):769–783

    Article  CAS  Google Scholar 

  • Chibani-Chennoufi S, Sidoti J, Bruttin A, Kutter E, Sarker S, Brüssow H (2004) In vitro and in vivo bacteriolytic activities of Escherichia coli phages: implications for phage therapy. Antimicrob Agents Chemother 48(7):2558–2569

    Article  CAS  Google Scholar 

  • Chibeu A, Lingohr EJ, Masson L, Manges A, Harel J, Ackermann HW, Boerlin P (2012) Bacteriophages with the ability to degrade uropathogenic Escherichia coli biofilms. Viruses 4(4):471–487

    Article  CAS  Google Scholar 

  • Comeau AM, Tétart F, Trojet SN, Prere MF, Krisch HM (2007) Phage-antibiotic synergy (PAS): beta-lactam and quinolone antibiotics stimulate virulent phage growth. PLoS ONE 2(8):e799

    Article  Google Scholar 

  • Corbin BD, McLean RJ, Aron GM (2001) Bacteriophage T4 multiplication in a glucose-limited Escherichia coli biofilm. Can J Microbiol 47(7):680–684

    Article  CAS  Google Scholar 

  • Cornelissen A, Ceyssens PJ, T’Syen J, Van Praet H, Noben JP, Shaburova OV, Lavigne R (2011) The T7-related Pseudomonas putida phage phi15 displays virion-associated biofilm degradation properties. PLoS ONE 6(4):e18597

    Article  CAS  Google Scholar 

  • Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284(5418):1318–1322

    Article  CAS  Google Scholar 

  • Curtin JJ, Donlan RM (2006) Using bacteriophages to reduce formation of catheter-associated biofilms by Staphylococcus epidermidis. Antimicrob Agents Chemother 50(4):1268–1275

    Article  CAS  Google Scholar 

  • Dabrowska K, Switała-Jelen K, Opolski A, Weber-Dabrowska B, Gorski A (2005) Bacteriophage penetration in vertebrates. J Appl Microbiol 98(1):7–13

    Article  CAS  Google Scholar 

  • Donlan RM (2009) Preventing biofilms of clinically relevant organisms using bacteriophage. Trends Microbiol 17(2):66–72

    Article  CAS  Google Scholar 

  • Doolittle MM, Cooney JJ, Caldwell DE (1996) Tracing the interaction of bacteriophage with bacterial biofilms using fluorescent and chromogenic probes. J Ind Microbiol 16(6):331–341

    Article  CAS  Google Scholar 

  • Drulis-Kawa Z, Majkowska-Skrobek G, Maciejewska B, Delattre AS, Lavigne R (2012) Learning from bacteriophages-advantages and limitations of phage and phage-encoded protein applications. Curr Protein Pept Sci 13(8):699

    Article  CAS  Google Scholar 

  • Edgar R, Friedman N, Molshanski-Mor S, Qimron U (2012) Reversing bacterial resistance to antibiotics by phage-mediated delivery of dominant sensitive genes. Appl Environ Microbiol 78(3):744–751

    Article  CAS  Google Scholar 

  • Fischetti VA (2005) Bacteriophage lytic enzymes: novel anti-infectives. Trends Microbiol 13(10):491–496

    Article  CAS  Google Scholar 

  • Fu W, Forster T, Mayer O, Curtin JJ, Lehman SM, Donlan RM (2010) Bacteriophage cocktail for the prevention of biofilm formation by Pseudomonas aeruginosa on catheters in an in vitro model system. Antimicrob Agents Chemother 54(1):397–404

    Article  CAS  Google Scholar 

  • Garcia P, Madera C, Martínez B, Rodríguez A (2007) Biocontrol of staphylococcus aureus in curd manufacturing processes using bacteriophages. Int Dairy J 17(10):1232–1239

    Article  CAS  Google Scholar 

  • Glonti T, Chanishvili N, Taylor PW (2010) Bacteriophage-derived enzyme that depolymerizes the alginic acid capsule associated with cystic fibrosis isolates of Pseudomonas aeruginosa. J Appl Microbiol 108(2):695–702

    Article  CAS  Google Scholar 

  • Goldman G, Starosvetsky J, Armon R (2009) Inhibition of biofilm formation on UF membrane by use of specific bacteriophages. J Membr Sci 342(1):145–152

    Article  CAS  Google Scholar 

  • Goodridge LD (2010) Designing phage therapeutics. Curr Pharm Biotechnol 11(1):15–27

    Article  CAS  Google Scholar 

  • Gu J, Liu X, Li Y, Han W, Lei L, Yang Y, Feng X (2012) A method for generation phage cocktail with great therapeutic potential. PLoS ONE 7(3):e31698

    Article  CAS  Google Scholar 

  • Guttman B, Raya R, Kutter E (2004) Basic phage biology. In: Bacteriophages: biology and applications. CRC Press, pp 30–32

  • Hagens S, Habel A, Von Ahsen U, Von Gabain A, Bläsi U (2004) Therapy of experimental pseudomonas infections with a nonreplicating genetically modified phage. Antimicrob Agents Chemother 48(10):3817–3822

    Article  CAS  Google Scholar 

  • Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2(2):95–108

    Article  CAS  Google Scholar 

  • Hanlon GW (2007) Bacteriophages: an appraisal of their role in the treatment of bacterial infections. Int J Antimicrob Agents 30(2):118–128

    Article  CAS  Google Scholar 

  • Hanlon GW, Denyer SP, Olliff CJ, Ibrahim LJ (2001) Reduction in exopolysaccharide viscosity as an aid to bacteriophage penetration through Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 67(6):2746–2753

    Article  CAS  Google Scholar 

  • Harper DR, Parracho HM, Walker J, Sharp R, Hughes G, Werthén M, Lehman S, Morales S (2014) Bacteriophages biofilms. Antibiotics 3(3):270–284

    Article  CAS  Google Scholar 

  • Hermoso JA, García JL, García P (2007) Taking aim on bacterial pathogens: from phage therapy to enzybiotics. Curr Opin Microbiol 10(5):461–472

    Article  CAS  Google Scholar 

  • Herzberg M, Kang S, Elimelech M (2009) Role of extracellular polymeric substances (EPS) in biofouling of reverse osmosis membranes. Environ Sci Technol 43(12):4393–4398

    Article  CAS  Google Scholar 

  • Hibma AM, Jassim SA, Griffiths MW (1997) Infection and removal of L-forms of Listeria monocytogenes with bred bacteriophage. Int J Food Microbiol 34(3):197–207

    Article  CAS  Google Scholar 

  • Kiro R, Shitrit D, Qimron U (2014) Efficient engineering of a bacteriophage genome using the type IE CRISPR-Cas system. RNA Biol 11(1):42–44

    Article  CAS  Google Scholar 

  • Kocharunchitt C, Ross T, McNeil DL (2009) Use of bacteriophages as biocontrol agents to control Salmonella associated with seed sprouts. Int J Food Microbiol 128(3):453–459

    Article  CAS  Google Scholar 

  • Koskella B, Meaden S (2013) Understanding bacteriophage specificity in natural microbial communities. Viruses 5(3):806–823

    Article  Google Scholar 

  • Krogfelt KA, Poulsen LK, Molin S (1993) Identification of coccoid Escherichia coli BJ4 cells in the large intestine of streptomycin-treated mice. Infect Immun 61(12):5029–5034

    CAS  Google Scholar 

  • Kutter E (2005) Phage therapy: bacteriophages as natural, self-limiting antibiotics. Textb Nat Med 1:1147–1161

    Google Scholar 

  • Kutter E, De Vos D, Gvasalia G, Alavidze Z, Gogokhia L, Kuhl S, Abedon ST (2010) Phage therapy in clinical practice: treatment of human infections. Curr Pharm Biotechnol 11(1):69–86

    Article  CAS  Google Scholar 

  • Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8(5):317–327

    Article  CAS  Google Scholar 

  • Lajoie CA, Layton AC, Gregory IR, Sayler GS, Taylor DE, Meyers AJ (2000) Zoogleal clusters and sludge dewatering potential in an industrial activated-sludge wastewater treatment plant. Water Environ Res 72(1):56–64

    Article  CAS  Google Scholar 

  • Le-Clech P, Chen V, Fane TA (2006) Fouling in membrane bioreactors used in wastewater treatment. J Membr Sci 284(1):17–53

    Article  CAS  Google Scholar 

  • Leiman PG, Chipman PR, Kostyuchenko VA, Mesyanzhinov VV, Rossmann MG (2004) Three-dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host. Cell 118(4):419–429

    Article  CAS  Google Scholar 

  • Letarov AV, Golomidova AK, Tarasyan KK (2010) Ecological basis for rational phage therapy. Acta Nat 2(1):60

    CAS  Google Scholar 

  • Lidmar J, Mirny L, Nelson DR (2003) Virus shapes and buckling transitions in spherical shells. Phys Rev E 68(5):051910

    Article  Google Scholar 

  • Lin TY, Lo YH, Tseng PW, Chang SF, Lin YT, Chen TS (2012) A T3 and T7 recombinant phage acquires efficient adsorption and a broader host range. PLoS ONE 7(2):e30954

    Article  CAS  Google Scholar 

  • Liu M, Deora R, Doulatov SR, Gingery M, Eiserling FA, Preston A, Maskell DJ, Simons RW, Cotter PA, Parkhill J, Miller JF (2002) Reverse transcriptase-mediated tropism switching in Bordetella bacteriophage. Science 295(5562):2091–2094

    Article  CAS  Google Scholar 

  • Lodish H, Berk A, Zipursky SL, Matsudaira P, Baltimore D, Darnell J (2000) Section 6.3, viruses: structure, function, and uses. In: Molecular cell biology, 4th edn. New York

  • Loiselle M, Anderson KW (2003) The use of cellulase in inhibiting biofilm formation from organisms commonly found on medical implants. Biofouling 19(2):77–85

    Article  CAS  Google Scholar 

  • Lu TK, Collins JJ (2007) Dispersing biofilms with engineered enzymatic bacteriophage. Proc Natl Acad Sci 104(27):11197–11202

    Article  CAS  Google Scholar 

  • Lu TK, Collins JJ (2009) Engineered bacteriophage targeting gene networks as adjuvants for antibiotic therapy. Proc Natl Acad Sci 106(12):4629–4634

    Article  CAS  Google Scholar 

  • Mahichi F, Synnott AJ, Yamamichi K, Osada T, Tanji Y (2009) Site-specific recombination of T2 phage using IP008 long tail fiber genes provides a targeted method for expanding host range while retaining lytic activity. FEMS Microbiol Lett 295(2):211–217

    Article  CAS  Google Scholar 

  • Maiques E, Úbeda C, Tormo MÁ, Ferrer MD, Lasa Í, Novick RP, Penadés JR (2007) Role of staphylococcal phage and SaPI integrase in intra-and interspecies SaPI transfer. J Bacteriol 189(15):5608–5616

    Article  CAS  Google Scholar 

  • Matsuda T, Freeman TA, Hilbert DW, Duff M, Fuortes M, Stapleton PP, Daly JM (2005) Lysis-deficient bacteriophage therapy decreases endotoxin and inflammatory mediator release and improves survival in a murine peritonitis model. Surgery 137(6):639–646

    Article  Google Scholar 

  • Merril CR, Biswas B, Carlton R, Jensen NC, Creed GJ, Zullo S, Adhya S (1996) Long-circulating bacteriophage as antibacterial agents. Proc Natl Acad Sci 93(8):3188–3192

    Article  CAS  Google Scholar 

  • Merril CR, Scholl D, Adhya SL (2003) The prospect for bacteriophage therapy in Western medicine. Nat Rev Drug Discov 2(6):489–497

    Article  CAS  Google Scholar 

  • Modi SR, Collins JJ, Relman DA (2014) Antibiotics and the gut microbiota. J Clin Invest 124(10):4212–4218

    Article  CAS  Google Scholar 

  • Motlagh AM, Goel R (2014) Sustainability of activated sludge processes. Water reclamation and sustainability. Elsevier Science Ltd, Waltham, pp 391–414

    Book  Google Scholar 

  • Motlagh AM, Pant S, Gruden C (2013) The impact of cell metabolic activity on biofilm formation and flux decline during cross-flow filtration of ultrafiltration membranes. Desalination 316:85–90

    Article  CAS  Google Scholar 

  • Motlagh AM, Bhattacharjee AS, Goel R (2015) Microbiological study of bacteriophage induction in the presence of chemical stress factors in enhanced biological phosphorus removal (EBPR). Water Res 81:1–14

    Article  CAS  Google Scholar 

  • Musk J, Dinty J, Hergenrother PJ (2006) Chemical countermeasures for the control of bacterial biofilms: effective compounds and promising targets. Curr Med Chem 13(18):2163–2177

    Article  CAS  Google Scholar 

  • Nelson DC, Schmelcher M, Rodriguez-Rubio L, Klumpp J, Pritchard DG, Dong S, Donovan DM (2012) Endolysins as antimicrobials. Adv Virus Res 83:299–365

    Article  CAS  Google Scholar 

  • Nobrega FL, Costa AR, Kluskens LD, Azeredo J (2015) Revisiting phage therapy: new applications for old resources. Trends Microbiol 23(4):185–191

    Article  CAS  Google Scholar 

  • Orlova EV (2012) Bacteriophages and their structural organisation. In: Kurtboke I (ed) Bacteriophages. InTech, Rijeka, pp 3–30

  • O’Shea YA, Boyd EF (2002) Mobilization of the Vibrio pathogenicity island between Vibrio cholerae isolates mediated by CP-T1 generalized transduction. FEMS Microbiol Lett 214(2):153–157

    Article  Google Scholar 

  • Percival SL, Hill KE, Williams DW, Hooper SJ, Thomas DW, Costerton JW (2012) A review of the scientific evidence for biofilms in wounds. Wound Repair Regen 20(5):647–657

    Article  Google Scholar 

  • Poulsen LK, Licht TR, Rang C, Krogfelt KA, Molin S (1995) Physiological state of Escherichia coli BJ4 growing in the large intestines of streptomycin-treated mice. J Bacteriol 177(20):5840–5845

    CAS  Google Scholar 

  • Rapson ME, Burden FA, Glancy LP, Hodgson DA, Mann NH (2003) Bacteriophages useful for therapy and prophylaxis of bacterial infections. Patent WO03080823

  • Ryan EM, Alkawareek MY, Donnelly RF, Gilmore BF (2012) Synergistic phage-antibiotic combinations for the control of Escherichia coli biofilms in vitro. FEMS Immunol Med Microbiol 65(2):395–398

    Article  CAS  Google Scholar 

  • Sanin F, Vesilind P (1994) Effect of centrifugation on the removal of extracellular polymers and physical properties of activated sludge. Water Sci Technol 30(8):117–127

    CAS  Google Scholar 

  • Schmelcher M, Donovan DM, Loessner MJ (2012) Bacteriophage endolysins as novel antimicrobials. Future Microbiol 7(10):1147–1171

    Article  CAS  Google Scholar 

  • Scholl D, Adhya S, Merril C (2005) Escherichia coli K1’s capsule is a barrier to bacteriophage T7. Appl Environ Microbiol 71(8):4872–4874

    Article  CAS  Google Scholar 

  • Sidhu SS (2001) Engineering M13 for phage display. Biomol Eng 18(2):57–63

    Article  CAS  Google Scholar 

  • Sillankorva S, Oliveira R, Vieira MJ, Sutherland I, Azeredo J (2004) Bacteriophage Φ S1 infection of Pseudomonas fluorescens planktonic cells versus biofilms. Biofouling 20(3):133–138

    Article  Google Scholar 

  • Sillankorva S, Neubauer P, Azeredo J (2010) Phage control of dual species biofilms of Pseudomonas fluorescens and Staphylococcus lentus. Biofouling 26(5):567–575

    Article  Google Scholar 

  • Soni KA, Nannapaneni R (2010) Removal of Listeria monocytogenes biofilms with bacteriophage P100®. J Food Prot 73(8):1519–1524

    Google Scholar 

  • Srey S, Jahid IK, Ha SD (2013) Biofilm formation in food industries: a food safety concern. Food Control 31(2):572–585

    Article  Google Scholar 

  • Sulakvelidze A (2011) Bacteriophage: a new journal for the most ubiquitous organisms on Earth. Bacteriophage 1(1):1–2

    Article  Google Scholar 

  • Taylor EN, Webster TJ (2009) The use of superparamagnetic nanoparticles for prosthetic biofilm prevention. Int J Nanomed 4:145

    Article  CAS  Google Scholar 

  • Vitiello CL, Merril CR, Adhya S (2005) An amino acid substitution in a capsid protein enhances phage survival in mouse circulatory system more than a 1000-fold. Virus Res 114(1):101–103

    Article  CAS  Google Scholar 

  • Westwater C, Kasman LM, Schofield DA, Werner PA, Dolan JW, Schmidt MG, Norris JS (2003) Use of genetically engineered phage to deliver antimicrobial agents to bacteria: an alternative therapy for treatment of bacterial infections. Antimicrob Agents Chemother 47(4):1301–1307

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wittebole X, De Roock S, Opal SM (2014) A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence 5(1):226–235

    Article  Google Scholar 

  • Wu H, Moser C, Wang HZ, Høiby N, Song ZJ (2015) Strategies for combating bacterial biofilm infections. Int J Oral Sci 7(1):1–7

    Article  Google Scholar 

  • Xiong Y, Liu Y (2010) Biological control of microbial attachment: a promising alternative for mitigating membrane biofouling. Appl Microbiol Biotechnol 86(3):825–837

    Article  CAS  Google Scholar 

  • Yan J, Mao J, Xie J (2014) Bacteriophage polysaccharide depolymerases and biomedical applications. BioDrugs 28(3):265–274

    Article  CAS  Google Scholar 

  • Yoichi M, Abe M, Miyanaga K, Unno H, Tanji Y (2005) Alteration of tail fiber protein gp38 enables T2 phage to infect Escherichia coli O157: H7. J Biotechnol 115(1):101–107

    Article  CAS  Google Scholar 

  • Yosef I, Manor M, Kiro R, Qimron U (2015) Temperate and lytic bacteriophages programmed to sensitize and kill antibiotic-resistant bacteria. In: Proceedings of the national academy of sciences, 201500107

  • Zaky A, Escobar I, Motlagh AM, Gruden C (2012) Determining the influence of active cells and conditioning layer on early stage biofilm formation using cellulose acetate ultrafiltration membranes. Desalination 286:296–303

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We greatly appreciate the time reviewers have spent on this manuscript to provide their useful comments. This research was partially supported by National Science Foundation Grant #1055786. The views and rationale expressed in this manuscript are those of the authors and do not necessarily represent the funding agency.

Author information

Authors and Affiliations

  1. Department of Civil and Environmental Engineering, University of Utah, 110 S Central Campus Drive, Salt Lake City, 84112, UT, USA

    Amir Mohaghegh Motlagh, Ananda Shankar Bhattacharjee & Ramesh Goel

Authors
  1. Amir Mohaghegh Motlagh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ananda Shankar Bhattacharjee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ramesh Goel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ramesh Goel.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Motlagh, A.M., Bhattacharjee, A.S. & Goel, R. Biofilm control with natural and genetically-modified phages. World J Microbiol Biotechnol 32, 67 (2016). https://doi.org/10.1007/s11274-016-2009-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-016-2009-4

Keywords

Search

Navigation