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Control of Multidrug-Resistant Gene Flow in the Environment Through Bacteriophage Intervention

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Abstract

The spread of multidrug-resistant (MDR) bacteria is an emerging threat to the environment and public wellness. Inappropriate use and indiscriminate release of antibiotics in the environment through un-metabolized form create a scenario for the emergence of virulent pathogens and MDR bugs in the surroundings. Mechanisms underlying the spread of resistance include horizontal and vertical gene transfers causing the transmittance of MDR genes packed in different host, which pass across different food webs. Several controlling agents have been used for combating pathogens; however, the use of lytic bacteriophages proves to be one of the most eco-friendly due to their specificity, killing only target bacteria without damaging the indigenous beneficial flora of the habitat. Phages are part of the natural microflora present in different environmental niches and are remarkably stable in the environment. Diverse range of phage products, such as phage enzymes, phage peptides having antimicrobial properties, and phage cocktails also have been used to eradicate pathogens along with whole phages. Recently, the ability of phages to control pathogens has extended from the different areas of medicine, agriculture, aquaculture, food industry, and into the environment. To avoid the arrival of pre-antibiotic epoch, phage intervention proves to be a potential option to eradicate harmful pathogens generated by the MDR gene flow which are uneasy to cure by conventional treatments.

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Abbreviations

MDR:

Multidrug resistant

HGT:

Horizontal gene transfer

CETP:

Common effluent treatment plant

STP:

Sewage treatment plant

MRSA:

Methicillin-resistant Staphylococcus aureus

CRISPR:

Clustered regularly interspaced short palindromic repeats

References

  1. Taylor, D. (2015). The pharmaceutical industry and the future of drug development. Pharmaceuticals in the Environment, 1–33.

  2. Kalia, V. C. (2014). Microbes, antimicrobials and resistance: the battle goes on. Indian Journal of Microbiology, 54, 1–2.

    Article  CAS  Google Scholar 

  3. Sande-Bruinsma, N., Grundmann, H., Verloo, D., Tiemersma, E., Monen, J., & Goossens, H. (2008). Antimicrobial drug use and resistance in Europe. Emerging Infectious Diseases, 14(11), 1722–1730.

    Article  Google Scholar 

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

    Article  Google Scholar 

  5. Salmond, G. P., & Fineran, P. C. (2015). A century of the phage: past, present and future. Nature Reviews Microbiology, 13(12), 777–786.

    Article  CAS  Google Scholar 

  6. Borysowski, J., Lobocka, M., Miedzybrodzki, R., Weber-Dabrowska, B., & Gorski, A. (2011). Potential of bacteriophages and their lysins in the treatment of MRSA. Bio Drugs, 25(6), 347–355.

    CAS  Google Scholar 

  7. Czajkowski, R., Ozymko, Z., & Lojkowska, E. (2016). Application of zinc chloride precipitation method for rapid isolation and concentration of infectious Pectobacterium spp. and Dickeya spp. lytic bacteriophages from surface water and plant and soil extracts. Folia Microbiologica, 61(1), 29–33.

    Article  CAS  Google Scholar 

  8. Hausler, T. (2006). Viruses vs. superbugs. K. Leube, Trans. vol. 1, (pp. 1–292). New York: Macmillan. doi: 10.1007/978-0-230-55228-9.

  9. Lu, T. K., & Collins, J. J. (2009). Engineered bacteriophage targeting gene networks as adjuvants for antibiotic therapy. Proceedings of the National Academy of Sciences, USA, 106(12), 4629–4634.

    Article  CAS  Google Scholar 

  10. Kaur, S., Harjai, K., & Chhibber, S. (2012). Methicillin-resistant Staphylococcus aureus phage plaque size enhancement using sublethal concentrations of antibiotics. Applied and Environmental Microbiology, 78(23), 8227–8233.

    Article  CAS  Google Scholar 

  11. Endersen, L., O’Mahony, J., Hill, C., Ross, R. P., McAuliffe, O., & Coffey, A. (2014). Phage therapy in the food industry. Annual Review of Food Science and Technology, 5, 327–349.

    Article  CAS  Google Scholar 

  12. Andam, C. P., Carver, S. M., & Berthrong, S. T. (2015). Horizontal gene flow in managed ecosystems. Annual Review of Ecology, Evolution, and Systematics, 46, 121–143.

    Article  Google Scholar 

  13. Brown-Jaque, M., Calero-Cáceres, W., & Muniesa, M. (2015). Transfer of antibiotic-resistance genes via phage-related mobile elements. Plasmid, 7(9), 1–7.

    Article  CAS  Google Scholar 

  14. Fekadu, S., Merid, Y., Beyene, H., Teshome, W., & Gebre-Selassie, S. (2015). Assessment of antibiotic-and disinfectant-resistant bacteria in hospital wastewater, south Ethiopia: a cross-sectional study. The Journal of Infection in Developing Countries, 9(2), 149–156.

    Article  Google Scholar 

  15. Rizzo, L., Manaia, C., Merlin, C., Schwartz, T., Dagot, C., Ploy, M. C., & Fatta-Kassinos, D. (2013). Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Science of the Total Environment, 447, 345–360.

    Article  CAS  Google Scholar 

  16. Cox, G., & Wright, G. D. (2013). Intrinsic antibiotic resistance: mechanisms, origins, challenges and solutions. International Journal of Medical Microbiology, 303(6), 287–292.

    Article  CAS  Google Scholar 

  17. Li, X. Z., Plesiat, P., & Nikaido, H. (2015). The challenge of efflux-mediated antibiotic resistance in Gram-negative bacteria. Clinical Microbiology Reviews, 28(2), 337–418.

    Article  CAS  Google Scholar 

  18. Hermsen, R., Deris, J. B., & Hwa, T. (2012). On the rapidity of antibiotic resistance evolution facilitated by a concentration gradient. Proceedings of the National Academy of Sciences, 109(27), 10775–10780.

    Article  CAS  Google Scholar 

  19. Baysarowich, J., Koteva, K., Hughes, D. W., Ejim, L., Griffiths, E., Zhang, K., Junop, M., & Wright, G. D. (2008). Rifamycin antibiotic resistance by ADP-ribosylation: structure and diversity of Arr. Proceedings of the National Academy of Sciences, U. S. A, 105, 4886–4891.

    Article  CAS  Google Scholar 

  20. Ruppe, E., Woerther, P. L., & Barbier, F. (2015). Mechanisms of antimicrobial resistance in Gram-negative bacilli. Annals of Intensive Care, 5(1), 1.

    Article  CAS  Google Scholar 

  21. Berendonk, T. U., Manaia, C. M., Merlin, C., Fatta-Kassinos, D., Cytryn, E., Walsh, F., & Kreuzinger, N. (2015). Tackling antibiotic resistance: the environmental framework. Nature Reviews Microbiology, 13(5), 310–317.

    Article  CAS  Google Scholar 

  22. Arias, C. A., & Murray, B. E. (2009). Antibiotic-resistant bugs in the 21st century-a clinical super-challenge. The New England Journal of Medicine, 360(5), 439–443.

    Article  CAS  Google Scholar 

  23. Giamarellou, H. (2010). Multidrug-resistant Gram-negative bacteria: how to treat and for how long. International Journal of Antimicrobial Agents, 36, S50–S54.

    Article  CAS  Google Scholar 

  24. Hughes, K. A., Sutherland, I. W., Clark, J., & Jones, M. V. (1998). Bacteriophage and associated polysaccharide depolymerises-novel tools for study of bacterial biofilms. Journal of Applied Microbiology, 85(5), 83–90.

    Google Scholar 

  25. Popeda, M., Pluciennik, E., & Bednarek, A. K. (2013). Proteins in cancer multidrug resistance. Advances in Hygiene and Experimental Medicine, 68, 616–632.

    Google Scholar 

  26. Boucher, H. W., Talbot, G. H., Bradley, J. S., Edwards, J. E., Gilbert, D., Rice, L. B., & Bartlett, J. (2009). Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clinical Infectious Diseases, 48(1), 1–12.

    Article  Google Scholar 

  27. Klevens, R. M., Morrison, M. A., Nadle, J., Petit, S., Gershman, K., Ray, S., & Craig, A. S. (2007). Invasive methicillin-resistant Staphylococcus aureus infections in the United States. Journal of the American Medical Association, 298(15), 1763–1771.

    Article  CAS  Google Scholar 

  28. Allen, H. K., Donato, J., Wang, H. H., Cloud-Hansen, K. A., Davies, J., & Handelsman, J. (2010). Call of the wild: antibiotic resistance genes in natural environments. Nature Reviews Microbiology, 8(4), 251–259.

    Article  CAS  Google Scholar 

  29. Haque, M., Rahman, N. I. A., Zulkifli, Z., & Ismail, S. (2016). Antibiotic prescribing and resistance: knowledge level of medical students of clinical years of University Sultan Zainal Abidin, Malaysia. Journal of Therapeutics and Clinical Risk Management, 12, 413.

    Article  Google Scholar 

  30. De Vos, D., Pirnay, J. P., Bilocq, F., Jennes, S., Verbeken, G., Rose, T., & Heuninckx, W. (2016). Molecular epidemiology and clinical impact of Acinetobacter calcoaceticus-baumannii complex in a Belgian Burn Wound Center. PloS One, 11(5).

  31. Kalia, V. C., & Kumar, P. (2015). Genome wide search for biomarkers to diagnose Yersinia infections. Indian Journal of Microbiology, 55(4), 366–374.

    Article  CAS  Google Scholar 

  32. LaGier, M. J., & Threadgill, D. S. (2014). Identification and characterization of an invasion antigen B gene from the oral pathogen Campylobacter rectus. Indian Journal of Microbiology, 54(1), 33–40.

    Article  CAS  Google Scholar 

  33. Kong, W., Ye, J., Guan, S., Liu, J., & Pu, J. (2014). Epidemic status of swine influenza virus in China. Indian Journal of Microbiology, 54(1), 3–11.

    Article  Google Scholar 

  34. Mahale, K. N., Paranjape, P. S., Marathe, N. P., Dhotre, D. P., Chowdhury, S., Shetty, S. A., & Shouche, Y. S. (2014). Draft genome sequences of Yersinia pestis strains from the 1994 plague epidemic of Surat and 2002 Shimla outbreak in India. Indian Journal of Microbiology, 54(4), 480–482.

    Article  CAS  Google Scholar 

  35. Wang, M. Y., Shao, C., Li, J., Wang, X. Y., Wang, S. B., & Shao, S. H. (2015). Gene diversity of H. pylori cagPAI genes in patients with gastroduodenal diseases in a region at high risk of gastric cancer. Indian Journal of Microbiology, 55(1), 118–120.

    Article  CAS  Google Scholar 

  36. Saravanan, S., Purushothaman, V., Murthy, T. R. G. K., Sukumar, K., Srinivasan, P., Gowthaman, V., & Kuchipudi, S. V. (2015). Molecular epidemiology of nontyphoidal Salmonella in poultry and poultry products in India: implications for human health. Indian Journal of Microbiology, 55(3), 319–326.

    Article  CAS  Google Scholar 

  37. Van Bambeke, F., Glupczynski, Y., Plesiat, P., Pechere, J. C., & Tulkens, P. M. (2003). Antibiotic efflux pumps in prokaryotic cells: occurrence, impact on resistance and strategies for the future of antimicrobial therapy. Journal of Antimicrobial Chemotherapy, 51(5), 1055–1065.

    Article  CAS  Google Scholar 

  38. Li, X. Z., & Nikaido, H. (2009). Efflux-mediated drug resistance in bacteria. Drugs, 69(12), 1555–1623.

    Article  CAS  Google Scholar 

  39. Stix, G. (2006). An antibiotic resistance fighter. Scientific American, 294(4), 80–83.

    Article  Google Scholar 

  40. Dafale, N. A., Hathi, Z. J., Bit, S., & Purohit, H. J. (2015). Bacteriophage diversity in different habitats and their role in pathogen control. In Microbial Factories (Vol. 2, pp. 259–280). India: Springer.

    Chapter  Google Scholar 

  41. Koul, S., Prakash, J., Mishra, A., & Kalia, V. C. (2016). Potential emergence of multi-quorum sensing inhibitor resistant (MQSIR) bacteria. Indian Journal of Microbiology, 56(1), 1–18.

    Article  CAS  Google Scholar 

  42. Agarwala, M., Choudhury, B., & Yadav, R. N. S. (2014). Comparative study of antibiofilm activity of copper oxide and iron oxide nanoparticles against multidrug resistant biofilm forming uropathogens. Indian Journal of Microbiology, 54(3), 365–368.

    Article  CAS  Google Scholar 

  43. Li, X. Y., Yang, J. J., Mao, Z. C., Ho, H. H., Wu, Y. X., & He, Y. Q. (2014). Enhancement of biocontrol activities and cyclic lipopeptides production by chemical mutagenesis of Bacillus subtilis XF-1, a biocontrol agent of Plasmodiophorabrassicae and Fusariumsolani. Indian Journal of Microbiology, 54(4), 476–479.

    Article  CAS  Google Scholar 

  44. Pignanelli, S., Pulcrano, G., Iula, V. D., & Shurdhi, A. (2015). Anti-chlamydial IgG neutralizing ability in nonzoonotic atypical community acquired respiratory tract infections. Indian Journal of Microbiology, 55(3), 345–348.

    Article  CAS  Google Scholar 

  45. Saxena, A., Mukherjee, U., Kumari, R., Singh, P., & Lal, R. (2014). Synthetic biology in action: developing a drug against MDR-TB. Indian Journal of Microbiology, 54(4), 369–375.

    Article  CAS  Google Scholar 

  46. Alipiah, N. M., Shamsudin, M. N., Yusoff, F. M., & Arshad, A. (2015). Membrane biosynthesis gene disruption in methicillin-resistant Staphylococcus aureus (MRSA) as potential mechanism for reducing antibiotic resistance. Indian Journal of Microbiology, 55(1), 41–49.

    Article  CAS  Google Scholar 

  47. Cai, L., Zhao, X., Jiang, T., Qiu, J., Owusu, L., Ma, Y., & Xin, Y. (2014). Prokaryotic expression, identification and bioinformatics analysis of the Mycobacterium tuberculosis Rv3807c gene encoding the putative enzyme committed to decaprenylphosphoryl-D-arabinose synthesis. Indian Journal of Microbiology, 54(1), 46–51.

    Article  CAS  Google Scholar 

  48. Jeyanthi, V., & Velusamy, P. (2016). Anti-methicillin resistant Staphylococcus aureus compound isolation from halophilic Bacillus amyloliquefaciens MHB1 and determination of its mode of action using electron microscope and flow cytometry analysis. Indian Journal of Microbiology, 56(2), 148–157.

    Article  CAS  Google Scholar 

  49. Phong, T. Q., Volker, U., & Hammer, E. (2015). Using a label free quantitative proteomics approach to identify changes in protein abundance in multidrug-resistant Mycobacterium tuberculosis. Indian Journal of Microbiology, 55(2), 219–230.

    Article  CAS  Google Scholar 

  50. Ackermann, H. W., & Prangishvili, D. (2012). Prokaryote viruses studied by electron microscopy. Archives of Virology, 157(10), 1843–1849.

    Article  CAS  Google Scholar 

  51. Weinbauer, M. G. (2004). Ecology of prokaryotic viruses. Federation of European Microbiological Societies Microbiology Review, 28(2), 127–181.

    CAS  Google Scholar 

  52. Drulis-Kawa, Z., Majkowska-Skrobek, G., Maciejewska, B., Delattre, A. S., & Lavigne, R. (2012). Learning from bacteriophages-advantages and limitations of phage and phage-encoded protein applications. Current Protein and Peptide Science, 13(8), 699–722.

    Article  CAS  Google Scholar 

  53. Lorch, A. (1999). Bacteriophages: an alternative to antibiotics. Biotechnology and Development Monitoring, 39, 14–17.

    Google Scholar 

  54. Gravitz, L. (2012). Turning a new phage. Nature Medicine, 18(9), 1318–1320.

    Article  CAS  Google Scholar 

  55. Levin, B. R., & Bull, J. J. (2004). Population and evolutionary dynamics of phage therapy. Nature Reviews Microbiology, 2(2), 166–173.

    Article  CAS  Google Scholar 

  56. Viertel, T. M., Ritter, K., & Horz, H. P. (2014). Viruses versus bacteria-novel approaches to phage therapy as a tool against multidrug-resistant pathogens. Journal of Antimicrobial Chemotherapy, 69(9), 2326–2336.

    Article  CAS  Google Scholar 

  57. Gupta, R., & Prasad, Y. (2011). Efficacy of polyvalent bacteriophage P-27/HP to control multidrug resistant Staphylococcus aureus associated with human infections. Current Microbiology, 62(1), 255–260.

    Article  CAS  Google Scholar 

  58. Loc-Carrillo, C., & Abedon, S. T. (2011). Pros and cons of phage therapy. Bacteriophage, 1(2), 111–114.

    Article  Google Scholar 

  59. Melo, L. D., Sillankorva, S., Ackermann, H. W., Kropinski, A. M., Azeredo, J., & Cerca, N. (2014). Characterization of Staphylococcus epidermidis phage vB_SepS_SEP9–a unique member of the Siphoviridae family. Research in Microbiology, 165(8), 679–685.

    Article  CAS  Google Scholar 

  60. Abedon, S. T., Kuhl, S. J., Blasdel, B. G., & Kutter, E. M. (2011). Phage treatment of human infections. Bacteriophage, 1, 66–85.

    Article  Google Scholar 

  61. Mirzaei, M. K., Eriksson, H., Kasuga, K., Haggard-Ljungquist, E., & Nilsson, A. S. (2014). Genomic, proteomic, morphological, and phylogenetic analyses of vB_EcoP_SU10, a podoviridae phage with C3 morphology. PloS One, 9(12), e116294.

    Article  CAS  Google Scholar 

  62. Jun, J. W., Han, J. E., Tang, K. F., Lightner, D. V., Kim, J., Seo, S. W., & Park, S. C. (2016). Potential application of bacteriophage pVp-1: agent combating Vibrio parahaemolyticus strains associated with acute hepatopancreatic necrosis disease (AHPND) in shrimp. Aquaculture, 4(57), 100–103.

    Article  Google Scholar 

  63. Sarker, S. A., Sultana, S., Reuteler, G., Moine, D., Descombes, P., Charton, F., & Akter, M. (2016). Oral phage therapy of acute bacterial diarrhea with two coliphage preparations: a randomized trial in children from Bangladesh. eBioMedicine, 5(4), 124–137.

    Article  Google Scholar 

  64. Hwang, J. Y., Kim, J. E., Song, Y. J., & Park, J. H. (2016). Safety of using Escherichia coli bacteriophages as a sanitizing agent based on inflammatory responses in rats. Food Science Biotechnoogy, 25(1), 355–360.

    Article  CAS  Google Scholar 

  65. Kishor, C., Mishra, R. R., Saraf, S. K., Kumar, M., Srivastav, A. K., & Nath, G. (2016). Phage therapy of staphylococcal chronic osteomyelitis in experimental animal model. Indian Journal of Medicinal Research, 143(1), 87.

    Article  Google Scholar 

  66. Porter, J., Anderson, J., Carter, L., Donjacour, E., & Paros, M. (2016). In vitro evaluation of a novel bacteriophage cocktail as a preventative for bovine coliform mastitis. Journal of Dairy Sciences., 99(3), 2053–2062.

    Article  CAS  Google Scholar 

  67. Uimajuridze, A., Jvania, G., Chanishvili, N., Goderdzishvili, M., Sybesma, W., Managadze, L., & Kessler, T. (2016). 265 Phage therapy for the treatment for urinary tract infection: results of in-vitro screenings and in-vivo application using commercially available bacteriophage cocktails. Europeon Urology, 3(15), e265.

    Google Scholar 

  68. Kalatzis, P. G., Bastias, R., Kokkari, C., & Katharios, P. (2016). Isolation and characterization of two lytic bacteriophages, φSt2 and φGrn1; phage therapy application for biological control of Vibrio alginolyticus in aquaculture live feeds. PloS One, 11(3), e0151101.

    Article  CAS  Google Scholar 

  69. Leung, S. S., Parumasivam, T., Gao, F. G., Carrigy, N. B., Vehring, R., Finlay, W. H., & Chan, H. K. (2016). Production of inhalation phage powders using spray freeze drying and spray drying techniques for treatment of respiratory infections. Pharmaceutical Research, 33(6), 1486–1496.

    Article  CAS  Google Scholar 

  70. Jeon, J., D’Souza, R., Pinto, N., Ryu, C., Park, J., Yong, D., & Lee, K. (2016). Characterization and complete genome sequence analysis of two Myoviral bacteriophages infecting clinical carbapanem-resistant Acenitobacter baumannii isolates. Journal of Applied Microbiology., 121(1), 68–77.

    Article  CAS  Google Scholar 

  71. Semler, D. D., Goudie, A. D., Finlay, W. H., & Dennis, J. J. (2014). Aerosol phage therapy efficacy in Burkholderia cepacia complex respiratory infections. Antimicrobial Agents and Chemotherapy, 58(7), 4005–4013.

    Article  CAS  Google Scholar 

  72. Morello, E., Saussereau, E., Maura, D., Huerre, M., Touqui, L., & Debarbieux, L. (2011). Pulmonary bacteriophage therapy on Pseudomonas aeruginosa cystic fibrosis strains: first steps towards treatment and prevention. PloS One, 6(2), e16963.

    Article  CAS  Google Scholar 

  73. Colom, J., Cano-Sarabia, M., Otero, J., Cortes, P., Maspoch, D., & Llagostera, M. (2015). Liposome-encapsulated bacteriophages for enhanced oral phage therapy against Salmonella spp. Applied Environmental Microbiology, 81(14), 4841–4849.

    Article  CAS  Google Scholar 

  74. Wang, Y., Mi, Z., Niu, W., An, X., Yuan, X., Liu, H., & Zhang, X. (2016). Intranasal treatment with bacteriophage rescues mice from Acinetobacter baumannii-mediated pneumonia. Future Microbiology, 11(5), 631–641.

    Article  CAS  Google Scholar 

  75. Pouillot, F., Chomton, M., Blois, H., Courroux, C., Noelig, J., Bidet, P., Bingen, E., & Bonacorsi, S. (2012). Efficacy of bacteriophage therapy in experimental sepsis and meningitis caused by a clone O25b:H4-ST131 Escherichia coli strain producing CTX-M-15. Antimicrobial Agents and Chemotherapy, 56, 3568–3575.

    Article  CAS  Google Scholar 

  76. Sunagar, R., Patil, S. A., & Chandrakanth, R. K. (2010). Bacteriophage therapy for Staphylococcus aureus bacteremia in streptozotocin-induced diabetic mice. Research in Microbiology, 161(1), 854–860. doi:10.1016/j.resmic.2010.09.011.

    Article  Google Scholar 

  77. Hung, C. H., Kuo, C. F., Wang, C. H., Wu, C. M., & Tsao, N. (2011). Experimental phage therapy in treating Klebsiella pneumoniae-mediated liver abscesses and bacteremia in mice. Antimicrobial Agents and Chemotherapy, 55, 1358–1365. doi:10.1128/AAC.01123-10.

    Article  CAS  Google Scholar 

  78. Kumari, S., Harjai, K., & Chhibber, S. (2011). Bacteriophage versus antimicrobial agents for the treatment of murine burn wound infection caused by Klebsiella pneumonia B5055. Journal of Medical Microbiology, 60, 205–210. doi:10.1099/jmm.0.018580-0.

    Article  Google Scholar 

  79. Alemayehu, D., Casey, P. G., McAuliffe, O., Guinane, C. M., Martin, J. G., Shanahan, F., Coffey, A., Ross, R. P., & Hill, C. (2012). Bacteriophages φMR299-2 and φNH-4 can eliminate Pseudomonas aeruginosa in the murine lung and on cystic fibrosis lung airway cells. MBio, 3(2), e00029–e00012. doi:10.1128/mBio.00029-12.

    Article  CAS  Google Scholar 

  80. Yilmaz, C., Colak, M., Yilmaz, B. C., Ersoz, G., Kutateladze, M., & Gozlugol, M. (2013). Bacteriophage therapy in implant related infections: an experimental study. Journal of Bone and Joint Surgery American, 95, 117–125. doi:10.2106/JBJS.K.01135.

    Article  Google Scholar 

  81. Dafale, N., Lakhe, S., Yadav, K., Purohit, H., & Chakrabarti, T. (2008). Concentration and recovery of coliphages from water with bituminous coal. Water Environmental Research, 80(3), 282–288.

    Article  CAS  Google Scholar 

  82. Sulakvelidze, A., Alavidze, Z., & Morris, J. G. (2001). Bacteriophage therapy. Antimicrobial Agents and Chemotherapy, 45(3), 649–659.

    Article  CAS  Google Scholar 

  83. Dafale, N., Semwal, U., Rajput, R., & Singh, G. (2016). Selection of appropriate analytical tools to determine the potency, microbial bioactivity and antibiotic resistances. Journal of Pharmaceutical Analysis, 6(4), 207–213. doi:10.1016/j.jpha.2016.05.006.

    Article  Google Scholar 

  84. Dafale, N., Semwal, U., Agarwal, P., Sharma, P., & Singh, G. (2015). Development and validation of microbial bioassay for quantification of Levofloxacin in pharmaceutical preparations. Journal of Pharmaceutical Analysis, 5(1), 18–26.

    Article  CAS  Google Scholar 

  85. Uchiyama, T. I., Uchiyama, J., Kato, S. I., Inoue, T., Ujihara, T., Ohara, N., & Matsuzaki, S. (2013). Evaluating efficacy of bacteriophage therapy against Staphylococcus aureus infections using a silkworm larval infection model. FEMS Microbiology Letters, 347(1), 52–60.

    Article  CAS  Google Scholar 

  86. Kaur, G., Rajesh, S., & Princy, S. A. (2015). Plausible drug targets in the Streptococcus mutans quorum sensing pathways to combat dental biofilms and associated risks. Indian Journal of Microbiology, 55(4), 349–356.

    Article  CAS  Google Scholar 

  87. Hermoso, J. A., Garcia, J. L., & Garcia, P. (2007). Taking aim on bacterial pathogens: from phage therapy to enzybiotics. Current Opinions in Microbiology, 10(5), 461–472.

    Article  CAS  Google Scholar 

  88. Jassim, S. A., Limoges, R. G., & El-Cheikh, H. (2016). Bacteriophage biocontrol in wastewater treatment. World Journal Microbiology Biotechnology, 32(4), 1–10.

    Article  CAS  Google Scholar 

  89. Loessner, M. J., Kramer, K., Ebel, F., & Scherer, S. (2002). C-terminal domains of Listeria monocytogenes bacteriophage murein hydrolases determine specific recognition and high-affinity binding to bacterial cell wall carbohydrates. Molecular Microbiology, 44(2), 335–349.

    Article  CAS  Google Scholar 

  90. Moak, M., & Molineux, I. J. (2004). Peptidoglycan hydrolytic activities associated with bacteriophage virions. Molecular Microbiology, 51(4), 1169–1183.

    Article  CAS  Google Scholar 

  91. Nelson, D., Loomis, L., & Fischetti, V. A. (2001). Prevention and elimination of upper respiratory colonization of mice by group A streptococci by using a bacteriophage lytic enzyme. Proceedings of the National Academy of Sciences, USA, 98(7), 4107–4112.

    Article  CAS  Google Scholar 

  92. Yoong, P., Schuch, R., Nelson, D., & Fischetti, V. A. (2004). Identification of a broadly active phage lytic enzyme with lethal activity against antibiotic-resistant Enterococcus faecalis and Enterococcus faecium. Journal of Bacteriology, 186(14), 4808–4812.

    Article  CAS  Google Scholar 

  93. Schuch, R., Nelson, D., & Fischetti, V. A. (2002). A bacteriolytic agent that detects and kills Bacillus anthracis. Nature, 418(6900), 884–889.

    Article  CAS  Google Scholar 

  94. Jado, I., Lopez, R., Garcia, E., Fenoll, A., Casal, J., Garcia, P., & Spanish Pneumococcal Infection Study Network. (2003). Phage lytic enzymes as therapy for antibiotic-resistant Streptococcus pneumoniae infection in a murine sepsis model. Journal of Antimicrobial agents and Chemotherapy, 52(6), 967–973.

    Article  CAS  Google Scholar 

  95. Bernhardt, T. G., Struck, D. K., & Young, R. Y. (2001). The lysis protein E of φX174 is a specific inhibitor of the MraY-catalyzed step in peptidoglycan synthesis. Journal Biological Chemistry, 276(9), 6093–6097.

    Article  CAS  Google Scholar 

  96. Wright, A., Hawkins, C. H., Anggard, E. E., & Harper, D. R. (2009). A controlled clinical trial of a therapeutic bacteriophage preparation in chronic otitis due to antibiotic-resistant Pseudomonas aeruginosa; a preliminary report of efficacy. Clinical Otolaryngology and Allied Sciences, 34(4), 349–357.

    Article  CAS  Google Scholar 

  97. Monk, A. B., Rees, C. D., Barrow, P., Hagens, S., & Harper, D. R. (2010). Bacteriophage applications: where are we now? Letters in Applied Microbiology, 51(4), 363–369.

    Article  CAS  Google Scholar 

  98. Sulakvelidze, A. (2005). Phage therapy: an attractive option for dealing with antibiotic-resistant bacterial infections. Drug Discovery Today, 10(12), 807–809.

    Article  Google Scholar 

  99. Arisaka, F., Kanamaru, S., Leiman, P., & Rossmann, M. G. (2003). The tail lysosyme complex of bacteriophage T4. The International Journal of Biochemistry & Cell Biology, 35, 16–21.

    Article  CAS  Google Scholar 

  100. Milller, E. S., Kutter, E., Mosig, G., Arisaka, F., Kunisawa, T., & Ruger, W. (2003). Bacteriophage T4 genome. Microbiology and Molecular Biological Review, 67, 86–156.

    Article  CAS  Google Scholar 

  101. Rossmann, M. G., Mesyanzhiniov, V. V., Arisaka, F., & Leiman, P. G. (2004). The bacteriophage T4 DNA injection machine. Current Opinion in Structural Biology, 14, 171–180.

    Article  CAS  Google Scholar 

  102. Chhibber, S., Kaur, T., & Kaur, S. (2013). Co-therapy using lytic bacteriophage and linezolid: effective treatment in eliminating methicillin resistant Staphylococcus aureus (MRSA) from diabetic foot infections. PloS One, 8(2), e56022.

    Article  CAS  Google Scholar 

  103. Torres-Barcelo, C., Arias-Ssnchez, F. I., Vasse, M., Ramsayer, J., Kaltz, O., & Hochberg, M. E. (2014). A window of opportunity to control the bacterial pathogen Pseudomonas aeruginosa combining antibiotics and phages. PloS One, 9(9), e106628.

    Article  CAS  Google Scholar 

  104. Ryan, E. M., Alkawareek, M. Y., Donnelly, R. F., & Gilmore, B. F. (2012). Synergistic phage-antibiotic combinations for the control of Escherichia coli biofilms in vitro. FEMS Immunology and Medical Microbiology, 65(2), 395–398.

    Article  CAS  Google Scholar 

  105. Gui, Z., Wang, H., Ding, T., Zhu, W., Zhuang, X., & Chu, W. (2014). Azithromycin reduces the production of α-hemolysin and biofilm formation in Staphylococcus aureus. Indian Journal of Microbiology, 54(1), 114–117.

    Article  CAS  Google Scholar 

  106. Xia, F., Li, X., Wang, B., Gong, P., Xiao, F., Yang, M., & Sun, C. (2016). Combination therapy of LysGH15 and apigenin as a new strategy for treating pneumonia caused by Staphylococcus aureus. Applied and Environmental Microbiology, 82(1), 87–94.

    Article  CAS  Google Scholar 

  107. Abedon, S. T. (2012). Bacterial immunity against bacteriophages. Bacteriophage, 2(1), 50–54.

    Article  Google Scholar 

  108. 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. Journal of Bacteriology, 169(12), 5429–5433.

    Article  CAS  Google Scholar 

  109. Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., & Horvath, P. (2007). CRISPR provides acquired resistance against viruses in prokaryotes. Science, 315(5819), 1709–1712.

    Article  CAS  Google Scholar 

  110. Brouns, S. J., Jore, M. M., Lundgren, M., Westra, E. R., Slijkhuis, R. J., Snijders, A. P., & Van Der Oost, J. (2008). Small CRISPR RNAs guide antiviral defense in prokaryotes. Science, 321(5891), 960–964.

    Article  CAS  Google Scholar 

  111. Hale, C. R., Zhao, P., Olson, S., Duff, M. O., Graveley, B. R., Wells, L., & Terns, M. P. (2009). RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell, 139(5), 945–956.

    Article  CAS  Google Scholar 

  112. Nigam, A., Gupta, D., & Sharma, A. (2014). Treatment of infectious disease: beyond antibiotics. Microbiological Research, 169, 643–651.

    Article  CAS  Google Scholar 

  113. Bondy-Denomy, J., Pawluk, A., Maxwell, K. L., & Davidson, A. R. (2013). Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature, 493(7432), 429–432.

    Article  CAS  Google Scholar 

  114. Pawluk, A., Bondy-Denomy, J., Cheung, V. H., Maxwell, K. L., & Davidson, A. R. (2014). A new group of phage anti-CRISPR genes inhibits the type IE CRISPR-Cas system of Pseudomonas aeruginosa. MBio, 5(2), e00896–e00814.

    Article  CAS  Google Scholar 

  115. Bondy-Denomy, J., Garcia, B., Strum, S., Du, M., Rollins, M. F., Hidalgo-Reyes, Y., & Davidson, A. R. (2015). Multiple mechanisms for CRISPR-Cas inhibition by anti-CRISPR proteins. Nature, 526, 136–139.

    Article  CAS  Google Scholar 

  116. Maxwell, K. L. (2016). Phages fight back: inactivation of the CRISPR-Cas bacterial immune system by anti-CRISPR proteins. PLoS Pathogens, 12(1), e1005282. doi:10.1371/journal.ppat.1005282.

    Article  CAS  Google Scholar 

  117. Yosef, I., Manor, M., Kiro, R., & Qimron, U. (2015). Temperate and lytic bacteriophages programmed to sensitize and kill antibiotic resistant bacteria. Proceedings of the National Academy of Sciences, USA, 112, 7267–7272.

    Article  CAS  Google Scholar 

  118. Matsuda, T., Freeman, T. A., & Hilbert, D. W. (2005). Lysis-deficient bacteriophage therapy decreases endotoxin and inflammatory mediator release and improves survival in a murine peritonitis model. Surgery, 137, 639–646.

    Article  Google Scholar 

  119. Broussard, G. W., Oldfield, L. M., Villanueva, V. M., Lunt, B. L., Shine, E. E., & Hatfull, G. F. (2013). Integration-dependent bacteriophage immunity provides insights into the evolution of genetic switches. Molecular Cell, 49(2), 237–248.

    Article  CAS  Google Scholar 

  120. Edgar, R., Friedman, N., Molshanski-Mor, S., & Qimron, U. (2012). Reversing bacterial resistance to antibiotics by phage mediated delivery of dominant sensitive genes. Applied Environmental Microbiology, 78, 744–751. doi:10.1128/AEM.05741-11.

    Article  CAS  Google Scholar 

  121. Kingston, J. J., Majumder, S., Uppalapati, S. R., Makam, S. S., Urs, R. M., Murali, H. S., & Batra, H. V. (2015). Anthrax outbreak among cattle and its detection by extractable antigen 1 (EA1) based sandwich ELISA and immuno PCR. Indian Journal of Microbiology, 55(1), 29–34.

    Article  CAS  Google Scholar 

  122. Wittebole, X., De Roock, S., & Opal, S. M. (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 

  123. Alisky, J., Iczkowski, K., Rapoport, A., & Troitsky, N. (1998). Bacteriophages show promise as antimicrobial agents. Journal of Infection, 36(1), 5–15.

    Article  CAS  Google Scholar 

  124. Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., & Zhang, F. (2013). Multiplex genome engineering using CRISPR/Cas systems. Science, 339(6121), 819–823.

    Article  CAS  Google Scholar 

  125. Seed, K. D., Lazinski, D. W., Calderwood, S. B., & Camilli, A. (2013). A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature, 494(7438), 489–491.

    Article  CAS  Google Scholar 

  126. Courchesne, N. M., Parisien, A., & Lan, C. Q. (2009). Production and application of bacteriophage and bacteriophage-encoded lysins. Recent Patents on Biotechnology, 3, 37–45.

    Article  CAS  Google Scholar 

  127. Matsuzaki, K., Sugishita, K. I., Harada, M., Fujii, N., & Miyajima, K. (1997). Interactions of an antimicrobial peptide, magainin 2, with outer and inner membranes of Gram-negative bacteria. BBA Biomembranes, 1327(1), 119–130.

    Article  CAS  Google Scholar 

  128. Jonczyk, E., Klak, M., Miedzybrodzki, R., & Gorski, A. (2011). The influence of external factors on bacteriophages-review. Folia Microbiologica, 56(3), 191–200.

    Article  CAS  Google Scholar 

  129. Bardina, C., Spricigo, D. A., Cortes, P., & Llagostera, M. (2012). Significance of the bacteriophage treatment schedule in reducing Salmonella colonization of poultry. Applied Environmental Microbiology, 78(18), 6600–6607.

    Article  CAS  Google Scholar 

  130. Gorski, A., Wazna, E., Dabrowska, B. W., Dabrowska, K., Switała-Jelen, K., & Miedzybrodzki, R. (2006). Bacteriophage translocation. FEMS Immunology and Medical Microbiology, 46(3), 313–319.

    Article  CAS  Google Scholar 

  131. Pirofski, L. A., & Casadevall, A. (1998). Use of licensed vaccines for active immunization of the immunocompromised host. Clinical Microbiology Reviews, 11(1), 1–26.

    CAS  Google Scholar 

  132. Azeredo, J., & Sutherland, I. W. (2008). The use of phages for the removal of infectious biofilms. Current Pharmaceutical Biotechnology, 9(4), 261–266.

    Article  CAS  Google Scholar 

  133. Cairns, B. J., & Payne, R. J. (2008). Bacteriophage therapy and the mutant selection window. Antimicrobial Agents and Chemotherapy, 52(12), 4344–4350.

    Article  CAS  Google Scholar 

  134. Merabishvili, M., Pirnay, J. P., Verbeken, G., Chanishvili, N., Tediashvili, M., Lashkhi, N., & Lavigne, R. (2009). Quality-controlled small-scale production of a well-defined bacteriophage cocktail for use in human clinical trials. PloS One, 4(3), e4944.

    Article  CAS  Google Scholar 

  135. Miedzybrodzki, R., Borysowski, J., Weber-Dabrowska, B., Fortuna, W., Letkiewicz, S., Szufnarowski, K., & Gorski, A. (2012). Clinical aspects of phage therapy. Advances in Virus Research, 83, 73.

    Article  CAS  Google Scholar 

  136. Kutter, E., De Vos, D., Gvasalia, G., Alavidze, Z., Gogokhia, L., Kuhl, S., & Abedon, S. T. (2010). Phage therapy in clinical practice: treatment of human infections. Current Pharmaceutical Biotechnology, 11(1), 69–86.

    Article  CAS  Google Scholar 

  137. Skurnik, M., Pajunen, M., & Kiljunen, S. (2007). Biotechnological challenges of phage therapy. Biotechnology Letters, 29(7), 995–1003.

    Article  CAS  Google Scholar 

  138. Jensen, E. C., Schrader, H. S., Rieland, B., Thompson, T. L., Lee, K. W., Nickerson, K. W., & Kokjohn, T. A. (1998). Prevalence of broad-host-range lytic bacteriophages of Sphaerotilus natans, Escherichia coli, and Pseudomonas aeruginosa. Applied Environmental Microbiology, 64(2), 575–580.

    CAS  Google Scholar 

  139. O’flaherty, S., Coffey, A., Meaney, W., Fitzgerald, G. F., & Ross, R. P. (2005). The recombinant phage lysinLysK has a broad spectrum of lytic activity against clinically relevant staphylococci, including methicillin-resistant Staphylococcus aureus. Journal Bacteriology, 187(20), 7161–7164.

    Article  CAS  Google Scholar 

  140. Loeffler, J. M., Djurkovic, S., & Fischetti, V. A. (2003). Phage lytic enzyme Cpl-1 as a novel antimicrobial for pneumococcal bacteremia. Infection and Immunity, 71, 6199–6204.

    Article  CAS  Google Scholar 

  141. Koul, S., Kumar, P., & Kalia, V. C. (2015). A unique genome wide approach to search novel markers for rapid identification of bacterial pathogens. Journal of Molecular and Genetic Medicine, 9, 194. doi:10.4172/1747-0862.1000194.

    Article  Google Scholar 

  142. Kekre, A., Bhushan, A., Kumar, P., & Kalia, V. C. (2015). Genome wide analysis for searching novel markers to rapidly identify Clostridium strains. Indian Journal of Microbiology, 55, 250–257. doi:10.1007/s12088-015-0535-7.

    Article  CAS  Google Scholar 

  143. Kalia, V. C., Kumar, P., Kumar, R., Mishra, A., & Koul, S. (2015). Genome wide analysis for rapid identification of Vibrio species. Indian Journal of Microbiology, 55, 375–383. doi:10.1007/s12088-015-0553-5.

    Article  Google Scholar 

  144. Kalia, V. C., Kumar, R., Kumar, P., & Koul, S. (2016). A genome-wide profiling strategy as an aid for searching unique identification biomarkers for Streptococcus. Indian Journal of Microbiology, 56, 46–58. doi:10.1007/s12088-015-0561-5.

    Article  CAS  Google Scholar 

  145. Kumar, R., Koul, S., Kumar, P., & Kalia, V. C. (2016). Searching biomarkers in the sequenced genomes of Staphylococcus for their rapid identification. Indian Journal of Microbiology, 56, 64–71. doi:10.1007/s12088-016-0565-9.

    Article  CAS  Google Scholar 

  146. Koul, S., & Kalia, V. C. (2016). Comparative genomics reveals biomarkers to identify Lactobacillus species. Indian Journal of Microbiology, 56, 253–263. doi:10.1007/s12088-016-0605-5.

    Google Scholar 

  147. Bhushan, A., Mukherjee, T., Joshi, J., Shankar, P., & Kalia, V. C. (2015). Insights into the origin of Clostridium botulinum strains: evolution of distinct restriction endonuclease sites in rrs (16S rRNA gene). Indian Journal of Microbiology, 55, 140–150. doi:10.1007/s12088-015-0514-z.

    Article  Google Scholar 

  148. More, R. P., Mitra, S., Raju, S. C., Kapley, A., & Purohit, H. J. (2014). Mining and assessment of catabolic pathways in the metagenome of a common effluent treatment plant to induce the degradative capacity of biomass. Bioresource Technology, 153, 137–146.

    Article  CAS  Google Scholar 

  149. Purohit, H. J., Raje, D. V., Kapley, A., Padmanabhan, P., & Singh, R. N. (2003). Peer reviewed: genomics tools in environmental impact assessment. Environmental Science and Technology, 37(19), 356A–363A.

    Article  Google Scholar 

  150. Paliwal, V., Puranik, S., & Purohit, H. J. (2012). Integrated perspective for effective bioremediation. Applied Biochemistry and Biotechnology, 166(4), 903–924.

    Article  CAS  Google Scholar 

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Acknowledgments

The authors are thankful to the Director, CSIR-National Environmental Engineering Research Institute, Nagpur for providing constant support, valuable guidance, and encouragements. Plagiarism has been checked using iThenticate software at CSIR-NEERI, Nagpur, and number is KRC\2016\SEP\EBGD\4.

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  1. Environmental Biotechnology and Genomics Division, CSIR-National Environmental Engineering Research Institute, Nagpur, 440020, India

    Krupa M. Parmar, Zubeen J. Hathi & Nishant A. Dafale

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  1. Krupa M. Parmar
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Parmar, K.M., Hathi, Z.J. & Dafale, N.A. Control of Multidrug-Resistant Gene Flow in the Environment Through Bacteriophage Intervention. Appl Biochem Biotechnol 181, 1007–1029 (2017). https://doi.org/10.1007/s12010-016-2265-7

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