1887

Abstract

We investigated the potential of bacteriophages alone as well as in combination with xylitol for tackling mixed-species biofilm of and . When mixed-species biofilm was established on polycarbonate discs, formed the base layer which was physically shielded on the top by Thereafter, mixed-species biofilm was treated with bacteriophages. -specific depolymerase-producing phage KPO1K2 caused significant reduction in the count of . In contrast, -specific non-depolymerase-producing phage Pa29 failed to cause any reduction in the count of . However, application of both phages together resulted in significant reduction in the count of both organisms. This suggests that depolymerase produced by phage KPO1K2 hydrolysed the top layer of and guided the entry of Pa29 to reach lying underneath. This phenomenon was confirmed when -specific non-depolymerase-producing phage NDP was used along with Pa29. Pa29 could not penetrate and reach its host bacterium. Xylitol worked synergistically along with the phage, resulting in a significant decrease in counts of both organisms. Disruption of mixed species biofilm by phage and xylitol was confirmed on the basis of the amount of protein and DNA released. This phage-based approach to altering the structural pattern and disrupting the mixed species biofilm is the first of its kind. It can be used as a topical application, a coating for foreign bodies or for aerosol delivery to tackle infections where both pathogens coexist in a biofilm mode.

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2015-07-01
2019-10-15
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References

  1. Abbas H.A. , Serry F.M. , El-Masry E.M. . ( 2012;). Synergic interaction between antibiotics and the artificial sweeteners xylitol and sorbitol against Pseudomonas aeruginosa biofilms. Asian J Pharm Res 2: 129–131.
    [Google Scholar]
  2. Adams M.H. . ( 1959;). Bacteriophages New York: Interscience Publishers;.
    [Google Scholar]
  3. Ammons M.C. , Ward L.S. , Fisher S.T. , Wolcott R.D. , James G.A. . ( 2009;). In vitro susceptibility of established biofilms composed of a clinical wound isolate of Pseudomonas aeruginosa treated with lactoferrin and xylitol. Int J Antimicrob Agents 33: 230–236 [CrossRef] [PubMed].
    [Google Scholar]
  4. An D. , Danhorn T. , Fuqua C. , Parsek M.R. . ( 2006;). Quorum sensing and motility mediate interactions between Pseudomonas aeruginosa Agrobacterium tumefaciens in biofilm cocultures. Proc Natl Acad Sci U S A 103: 3828–3833 [CrossRef] [PubMed].
    [Google Scholar]
  5. Anderl J.N. , Franklin M.J. , Stewart P.S. . ( 2000;). Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 44: 1818–1824 [CrossRef] [PubMed].
    [Google Scholar]
  6. Bedi M.S. , Verma V. , Chhibber S. . ( 2009;). Amoxicillin and specific bacteriophage can be used together for the eradication of biofilm of Klebsiella pneumoniae B5055. World J Microbiol Biotechnol 25: 1145–1151 [CrossRef].
    [Google Scholar]
  7. Ceri H. , Olson M.E. , Stremick C. , Read R.R. , Morck D. , Buret A. . ( 1999;). The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 37: 1771–1776 [PubMed].
    [Google Scholar]
  8. Chandrasekar P.H. , Manavathu E.K. . ( 2008;). Do Aspergillus species produce biofilm?. Future Microbiol 3: 19–21 [CrossRef] [PubMed].
    [Google Scholar]
  9. Childers B.M. , Van Laar T.A. , You T. , Clegg S. , Leung K.P. . ( 2013;). MrkD1P from Klebsiella pneumoniae strain IA565 allows for coexistence with Pseudomonas aeruginosa and protection from protease-mediated biofilm detachment. Infect Immun 81: 4112–4120 [CrossRef] [PubMed].
    [Google Scholar]
  10. Christensen B.B. , Haagensen J.A. , Heydorn A. , Molin S. . ( 2002;). Metabolic commensalism and competition in a two-species microbial consortium. Appl Environ Microbiol 68: 2495–2502 [CrossRef] [PubMed].
    [Google Scholar]
  11. Cox S.D. , Mann C.M. , Markham J.L. , Gustafson J.E. , Warmington J.R. , Wyllie S.G. . ( 2001;). Determining the antimicrobial actions of tea tree oil. Molecules 6: 87–91 [CrossRef].
    [Google Scholar]
  12. Donlan R.M. , Costerton J.W. . ( 2002;). Biofilms: survival mechanisms of clinically relevant micro-organisms. Clin Microbiol Rev 15: 167–193 [CrossRef] [PubMed].
    [Google Scholar]
  13. 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. Curr Protein Pept Sci 13: 699–722 [CrossRef] [PubMed].
    [Google Scholar]
  14. Filoche S.K. , Anderson S.A. , Sissons C.H. . ( 2004;). Biofilm growth of Lactobacillus species is promoted by Actinomyces species and Streptococcus mutans . Oral Microbiol Immunol 19: 322–326 [CrossRef] [PubMed].
    [Google Scholar]
  15. Furukawa H. , Kuroiwa T. , Mizushima S. . ( 1983;). DNA injection during bacteriophage tbl4 infection of Escherichia coli . J Bacteriol 154: 938–945 [PubMed].
    [Google Scholar]
  16. Ghezelbash G.R. , Nahvi I. , Rabbani M. . ( 2012;). Comparative inhibitory effect of xylitol and erythritol on the growth and biofilm formation of oral Streptococci . Afr J Microbiol Res 6: 4404–4408.
    [Google Scholar]
  17. Hall-Stoodley L. , Stoodley P. . ( 2005;). Biofilm formation and dispersal and the transmission of human pathogens. Trends Microbiol 13: 7–10 [CrossRef] [PubMed].
    [Google Scholar]
  18. Hughes K.A. , Sutherland I.W. , Jones M.V. . ( 1998;). Biofilm susceptibility to bacteriophage attack: the role of phage-borne polysaccharide depolymerase. Microbiology 144: 3039–3047 [CrossRef] [PubMed].
    [Google Scholar]
  19. Ichikawa T. , Yano Y. , Fujita Y. , Kashiwabara T. , Nagao K. . ( 2008;). The enhancement effect of three sugar alcohols on the fungicidal effect of benzethonium chloride toward Candida albicans . J Dent 36: 965–968 [CrossRef] [PubMed].
    [Google Scholar]
  20. Jung W.K. , Koo H.C. , Kim K.W. , Shin S. , Kim S.H. , Park Y.H. . ( 2008;). Antibacterial activity and mechanism of action of the silver ion in Staphylococcus aureus Escherichia coli . Appl Environ Microbiol 74: 2171–2178 [CrossRef] [PubMed].
    [Google Scholar]
  21. Kassa T. , Chhibber S. . ( 2012;). Thermal treatment of the bacteriophage lysate of Klebsiella pneumoniae B5055 as a step for the purification of capsular depolymerase enzyme. J Virol Methods 179: 135–141 [CrossRef] [PubMed].
    [Google Scholar]
  22. Kay M.K. , Erwin T.C. , McLean R.J.C. , Aron G.M. . ( 2011;). Bacteriophage ecology in Escherichia coli Pseudomonas aeruginosa mixed-biofilm communities. Appl Environ Microbiol 77: 821–829 [CrossRef] [PubMed].
    [Google Scholar]
  23. Knoll B.M. , Mylonakis E. . ( 2014;). Antibacterial bioagents based on principles of bacteriophage biology: an overview. Clin Infect Dis 58: 528–534 [CrossRef] [PubMed].
    [Google Scholar]
  24. Kumari S. , Harjai K. , Chhibber S. . ( 2009;). Characterization of Pseudomonas aeruginosa PAO specific bacteriophages isolated from sewage samples. Am J Biomed Sci 1: 91–102 [CrossRef].
    [Google Scholar]
  25. Luca M.D. , Maccari G. , Nifosi R. . ( 2014;). Treatment of Microbial Biofilms in the Post Antibiotic Era: Prophylactic and Therapeutic Use of Antimicrobial Peptides and Their Design by Bioinformatics Tools. Pathog Dis. 70: 257–270 [PubMed].[CrossRef]
    [Google Scholar]
  26. Lynch H. , Milgrom P. . ( 2003;). Xylitol and dental caries: an overview for clinicians. J Calif Dent Assoc 31: 205–209 [PubMed].
    [Google Scholar]
  27. Mäkinen K.K. , Söderling E.V.A. . ( 1980;). A quantitative study of mannitol, sorbitol, xylitol, and xylose in wild berries and commercial fruits. J Food Sci 45: 367–371 [CrossRef].
    [Google Scholar]
  28. Palmer R.J. Jr , Kazmerzak K. , Hansen M.C. , Kolenbrander P.E. . ( 2001;). Mutualism versus independence: strategies of mixed-species oral biofilms in vitro using saliva as the sole nutrient source. Infect Immun 69: 5794–5804 [CrossRef] [PubMed].
    [Google Scholar]
  29. Peters B.M. , Jabra-Rizk M.A. , O'May G.A. , Costerton J.W. , Shirtliff M.E. . ( 2012;). Polymicrobial interactions: impact on pathogenesis and human disease. Clin Microbiol Rev 25: 193–213 [CrossRef] [PubMed].
    [Google Scholar]
  30. Siebel M.A. , Characklis W.G. . ( 1991;). Observations of binary population biofilms. Biotechnol Bioeng 37: 778–789 [CrossRef] [PubMed].
    [Google Scholar]
  31. Sillankorva S. , Neubauer P. , Azeredo J. . ( 2010;). Phage control of dual species biofilms of Pseudomonas fluorescens Staphylococcus lentus . Biofouling 26: 567–575 [CrossRef] [PubMed].
    [Google Scholar]
  32. Stewart P.S. , Camper A.K. , Handran S.D. , Huang C. , Warnecke M. . ( 1997;). Spatial distribution and coexistence of Klebsiella pneumoniae Pseudomonas aeruginosa in biofilms. Microb Ecol 33: 2–10 [CrossRef] [PubMed].
    [Google Scholar]
  33. Thein Z.M. , Samaranayake Y.H. , Samaranayake L.P. . ( 2007;). Dietary sugars, serum and the biocide chlorhexidine digluconate modify the population and structural dynamics of mixed Candida albicans Escherichia coli biofilms. APMIS 115: 1241–1251 [CrossRef] [PubMed].
    [Google Scholar]
  34. Uhari M. , Tapiainen T. , Kontiokari T. . ( 2000;). Xylitol in preventing acute otitis media. Vaccine 19: (Suppl 1), S144–S147 [CrossRef] [PubMed].
    [Google Scholar]
  35. Verma V. , Harjai K. , Chhibber S. . ( 2009a;). Characterization of a tbl7-like lytic bacteriophage of Klebsiella pneumoniae B5055: a potential therapeutic agent. Curr Microbiol 59: 274–281 [CrossRef] [PubMed].
    [Google Scholar]
  36. Verma V. , Harjai K. , Chhibber S. . ( 2009b;). Restricting ciprofloxacin-induced resistant variant formation in biofilm of Klebsiella pneumoniae B5055 by complementary bacteriophage treatment. J Antimicrob Chemother 64: 1212–1218 [CrossRef] [PubMed].
    [Google Scholar]
  37. Wolcott R.D. , Rhoads D.D. , Bennett M.E. , Wolcott B.M. , Gogokhia L. , Costerton J.W. , Dowd S.E. . ( 2010;). Chronic wounds and the medical biofilm paradigm. J Wound Care 19: 45–46, 48–50, 52–53 [CrossRef] [PubMed].
    [Google Scholar]
  38. Yoshida S. , Ogawa N. , Fujii T. , Tsushima S. . ( 2009;). Enhanced biofilm formation and 3-chlorobenzoate degrading activity by the bacterial consortium of Burkholderia sp. NK8 and Pseudomonas aeruginosa PAO1. J Appl Microbiol 106: 790–800 [CrossRef] [PubMed].
    [Google Scholar]
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