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In Vitro Antibiofilm Activity of an Exopolysaccharide from the Marine Thermophilic Bacillus licheniformis T14

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Abstract

The development of antibiofilm strategies is of major interest in contrasting bacterial pathogenic biofilms. A novel fructose and fucose rich exopolysaccharide (EPS1-T14) produced by the recently described thermophilic Bacillus licheniformis T14, isolated from a shallow hydrothermal vent of Panarea Island (Eolian Island, Italy), was evaluated for its effects on biofilm formation by multiresistant clinical strains of Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, and Staphylococcus aureus. The antibiofilm activity of EPS1-T14 was assessed by microtiter plate assays and visualized by confocal laser scanning microscopic images. EPS1-T14, with molecular weight of 1000 kDa, reduced biofilm formation on abiotic surfaces without affecting bacterial vitality. The novel EPS1-T14 is a water-soluble, noncytotoxic exopolymer able to prevent biofilm formation and its use may represent a promising therapeutic strategy for combating bacterial biofilm-associated infections. EPS1-T14 as antiadhesive biomolecule could be useful for novel prospective in medical and nonmedical applications.

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References

  1. Arena A, Maugeri TL, Pavone B, Iannello D, Gugliandolo C, Bisignano G (2006) Antiviral and immunomodulatory effect of a novel exopolysaccharide from a marine thermotolerant Bacillus licheniformis. Int Immunopharmacol 6:8–13

    Article  CAS  PubMed  Google Scholar 

  2. Arena A, Gugliandolo C, Stassi G, Pavone B, Iannello D, Bisignano G, Maugeri TL (2009) An exopolysaccharide produced by Geobacillus thermodenitrificans strain B3-72: antiviral activity on immunocompetent cells. Immunol Lett 123:132–137

    Article  CAS  PubMed  Google Scholar 

  3. Bakkiyaraj D, Pandian SK (2010) In vitro and in vivo antibiofilm activity of a coral associated actinomycete against drug resistant Staphylococcus aureus biofilms. Biofouling 26:711–717

    Article  CAS  PubMed  Google Scholar 

  4. Bendaoud M, Vinogradov E, Balashova NV, Kadouri E, Kachlany SC, Kaplan JB (2011) Broad-spectrum biofilm inhibition by Kingella kingae exopolysaccharide. J Bacteriol 193:3879–3886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bramhachari PV, Dubey SK (2006) Isolation and characterization of exopolysaccharides produced by Vibrio harveyi strain VB23. Lett Appl Microbiol 43:571–577

    Article  CAS  PubMed  Google Scholar 

  6. Bridier A, Dubois-Brissonnet F, Boubetra A, Thomas V, Briandet R (2010) The biofilm architecture of sixty opportunistic pathogens deciphered using a high throughput CLSM method. J Microbiol Methods 82:64–70

    Article  CAS  PubMed  Google Scholar 

  7. Cao X-H, Liao Z-Y, Wang C-L, Yang W-Y, Lu M-F (2009) Evaluation of a lipopeptide biosurfactant from Bacillus natto TK-1 as a potential source of anti-adhesive, antimicrobial and antitumor activities. Braz J Microbiol 40:373–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Cescutti P, Kallioinen A, Impallomeni G, Toffanin R, Pollesello P, Leisola M, Eerikainen T (2005) Structure of the exopolysaccharide produced by Enterobacter amnigenus. Carbohydr Res 340:439–447

    Article  CAS  PubMed  Google Scholar 

  9. Clinical Laboratory Standards Institute (CLSI) (2006) Performance standards for antimicrobial susceptibility testing. In: 16th informational supplement, Wayne, PA

  10. Coffey BM, Anderson GG (2014) Biofilm formation in the 96-well microtiter plate. In: Pseudomonas methods and protocols, vol. 1149 of the series methods in molecular biology, Springer, New York, pp. 631–641

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

    Article  CAS  PubMed  Google Scholar 

  12. Das P, Mukherjee S, Sen R (2009) Substrate dependent production of extracellular biosurfactant by a marine bacterium. Bioresour Technol 100:1015–1019

    Article  CAS  PubMed  Google Scholar 

  13. Dheilly A, Soum-Soutera E, Klein GL, Bazire A, Compère C, Haras D, Dufour A (2010) Antibiofilm activity of the marine bacterium Pseudoalteromonas sp. strain 3J6. Appl Environ Microbiol 76:3452–3461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Dickschat JS (2010) Quorum sensing and bacterial biofilms. Nat Prod Rep 27:343–369

    Article  CAS  PubMed  Google Scholar 

  15. Di Lorenzo A, Varcamonti M, Parascandola P, Vignola R, Bernardi A, Sacceddu P, Sisto R, de Alteriis E (2005) Characterization and performance of a toluene-degrading biofilm developed on pumice stones. Microb Cell Fact 4:4

    Article  PubMed  PubMed Central  Google Scholar 

  16. Estrela AB, Heck MG, Abraham WR (2009) Novel approaches to control biofilm infections. Curr Med Chem 16:1512–1530

    Article  CAS  PubMed  Google Scholar 

  17. Flemming HC, Wingender J (2001) Relevance of microbial extracellular polymeric substances (EPSs)-Part I: structural and ecological aspects. Water Sci Technol 43:1–8

    CAS  PubMed  Google Scholar 

  18. Flemming HC, Neu TR, Wozniak DJ (2007) The EPS matrix: the “house of biofilm cells”. J Bacteriol 189:7945–7947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Freitas F, Alves VD, Torres CAV, Cruz M, Sousa I, Melo MJ, Ramos AM, Reis MAM (2011) Fucose-containing exopolysaccharide produced by the newly isolated Enterobacter strain A47 DSM23139. Carbohydr Polym 83:159–165

    Article  CAS  Google Scholar 

  20. Freitas F, Alves VD, Reis MAM (2011) Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends Biotechnol 29:388–398

    Article  CAS  PubMed  Google Scholar 

  21. Gugliandolo C, Lentini V, Spanò A, Maugeri TL (2012) New bacilli from shallow hydrothermal vents of Panarea Island (Italy) and their biotechnological potential. J Appl Microbiol 112:1102–1112

    Article  CAS  PubMed  Google Scholar 

  22. Gugliandolo C, Spanò A, Lentini V, Arena A, Maugeri TL (2014) Antiviral and immunomodulatory effects of a novel bacterial exopolysaccharide of shallow marine vent origin. J Appl Microbiol 116:1028–1034

    Article  CAS  PubMed  Google Scholar 

  23. Hoiby N, Ciofu O, Johansen HK, Song ZJ, Moser C, Jensen PO, Molin S, Givskov M, Tolker-Nielsen T, Bjarnsholt T (2011) The clinical impact of bacterial biofilms. Int J Oral Sci 3:55–65

    Article  PubMed  PubMed Central  Google Scholar 

  24. Imberty A, Wimmerova M, Mitchell EP, Gilboa-Garber N (2004) Structures of the lectins from Pseudomonas aeruginosa: insight into the molecular basis for host glycan recognition. Microbes Infect 6:221–228

    Article  CAS  PubMed  Google Scholar 

  25. Jiang P, Jiang P, Li J, Han F, Duan G, Lu X, Lu X, Gu Y, Yu W (2011) Antibiofilm activity of an exopolysaccharide from marine bacterium Vibrio sp. QY101. Plos One 6:e18514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Joshi S, Bharucha C, Jha S, Yadav S, Nerurkar A, Desai AJ (2008) Biosurfactant production using molasses and whey under thermophilic conditions. Bioresour Technol 99:195–199

    Article  CAS  PubMed  Google Scholar 

  27. Kanmani P, Satish Kumar R, Yuvaraj N, Paari KA, Pattukumar V, Arul V (2011) Production and purification of a novel exopolysaccharide from lactic acid bacterium Streptococcus phocae PI80 and its functional characteristics activity in vitro. Bioresour Technol 102:4827–4833

    Article  CAS  PubMed  Google Scholar 

  28. Kim Y, Oh S, Kim SH (2009) Released exopolysaccharide (r-EPS) produced from probiotic bacteria reduce biofilm formation of enterohemorrhagic Escherichia coli O157:H7. Biochem Biophys Res Commun 379:324–329

    Article  CAS  PubMed  Google Scholar 

  29. Klein GL, Soum-Soutera E, Guede Z, Bazire A, Compere C, Dufour A (2011) The anti-biofilm activity secreted by a marine Pseudoalteromonas strain. Biofouling 27:931–940

    Article  PubMed  Google Scholar 

  30. Kumar AS, Mody K, Jha B (2007) Bacterial exopolysaccharides–a perception. J Basic Microbiol 47:103–117

    Article  CAS  PubMed  Google Scholar 

  31. Laganà P, Caruso G, Mazzù F, Parisi S, Caruso G, Delia S (2015) Brief notes about Biofilm. In: Microbial Toxins and related contamination in the Food Industry—Springer Briefs in Molecular Sciences–Chemistry of Foods–Chapter: 3, pp.57–78

  32. Laganà P, Melcarne L, Delia S (2015) Acinetobacter baumannii and endocarditis, rare complication but important clinical relevance. Int J Cardiol 187:678–679

    Article  PubMed  Google Scholar 

  33. Liu C, Lu J, Lu L, Liu Y, Wanga F, Xiao M (2010) Isolation, structural characterization and immunological activity of an exopolysaccharide produced by Bacillus licheniformis 8-37-0-1. Bioresour Technol 101:5528–5533

    Article  CAS  PubMed  Google Scholar 

  34. Maugeri TL, Gugliandolo C, Caccamo D, Panico A, Lama L, Gambacorta A, Nicolaus B (2002) A halophilic thermotolerant Bacillus isolated from a marine hot spring able to produce a new exopolysaccharide. Biotechnol Lett 24:515–519

    Article  CAS  Google Scholar 

  35. Maugeri TL, Gugliandolo C, Caccamo D, Stackebrandt E (2002) Three novel halotolerant and thermophilic Geobacillus strains from shallow marine vents. Syst Appl Microbiol 25:450–455

    Article  CAS  PubMed  Google Scholar 

  36. Melo WCMA, Perussi JR (2013) Strategies to overcome biofilm resistance. In: Méndez-Vilas A (ed) Microbial pathogens and strategies for combating them: science, technology and education, vol 1. Formatex Research Center, pp 179–187

  37. Monroe D (2007) Looking for chinks in the armor of bacterial biofilms. PLoS Biol 5:e307

    Article  PubMed  PubMed Central  Google Scholar 

  38. Nicolaus B, Panico A, Manca MC, Lama L, Gambacorta A, Maugeri TL, Gugliandolo C, Caccamo D (2000) A thermophilic Bacillus isolated from an Eolian shallow hydrothermal vent, able to produce exopolysaccharides. Syst Appl Microbiol 23:426–432

    Article  CAS  PubMed  Google Scholar 

  39. Nicolaus B, Schiano Moriello V, Maugeri TL, Gugliandolo C, Gambacorta A (2003) Bacilli from shallow Mediterranean marine vents producers of exopolysaccharides. Recent Res Dev Microbiol 7:197–208

    CAS  Google Scholar 

  40. Nicolaus B, Kambourova M, Oner ET (2010) Exopolysaccharides from extremophiles: from fundamentals to biotechnology. Environ Technol 31:1145–1158

    Article  CAS  PubMed  Google Scholar 

  41. Nithya C, Devi MG, Pandian SK (2011) A novel compound from the marine bacterium Bacillus pumilus S6-15 inhibits biofilm formation in Gram-positive and Gram-negative species. Biofouling 27:519–528

    Article  CAS  PubMed  Google Scholar 

  42. Nithyanand P, Thenmozhi R, Rathna J, Pandian SK (2010) Inhibition of biofilm formation in Streptococcus pyogenes by coral associated Actinomycetes. Curr Microbiol 60:454–460

    Article  CAS  PubMed  Google Scholar 

  43. O’Toole GA (2011) Microtiter dish biofilm formation assay. J Vis Exp 30:2437

    Google Scholar 

  44. Papa R, Parrilli E, Sannino F, Barbato G, Tutino ML, Artini M, Selan L (2013) Anti-biofilm activity of the Antarctic marine bacterium Pseudoalteromonas haloplanktis TAC 125. Res Microbiol 164:450–456

    Article  CAS  PubMed  Google Scholar 

  45. Paul FMB, Perry DF, Monsan PF (1996) Strain of Klebsiella pneumoniae, subsp. pneumoniae, and a process for the production of a polysaccharide containing l-fucose. International Patent No. WO 9,623,057

  46. Péterszegi G, Fodil-Bourahla I, Robert AM, Robert L (2003) Pharmacological properties of fucose. Applications in age-related modifications of connective tissues. Biomed Pharmacother 57:240–245

    Article  PubMed  Google Scholar 

  47. Qin Z, Yang L, Qu D, Molin S, Tolker-Nielsen T (2009) Pseudomonas aeruginosa extracellular products inhibit staphylococcal growth, and disrupt established biofilms produced by Staphylococcus epidermidis. Microbiology 155:2148–2156

    Article  CAS  PubMed  Google Scholar 

  48. Rendueles O, Travier L, Latour-Lambert P, Fontaine T, Magnus J, Denamur E, Ghigo JM (2011) Screening of Escherichia coli species biodiversity reveals new biofilm-associated anti-adhesion polysaccharides. MBio 2:e00011–e00043

    Article  Google Scholar 

  49. Rendueles O, Kaplan JB, Ghigo J-M (2013) Antibiofilm polysaccharides. Environ Microbiol 15:334–346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Roca C, Alves VD, Freitas F, Reis MAM (2015) Exopolysaccharides enriched in rare sugars: bacterial sources, production, and applications. Front Microbiol 6:288

    Article  PubMed  PubMed Central  Google Scholar 

  51. Sayem SA, Manzo E, Ciavatta L, Tramice A, Cordone A, Zanfardino A, De Felice M, Varcamonti M (2011) Anti-biofilm activity of an exopolysaccharide from a sponge-associated strain of Bacillus licheniformis. Microb Cell Fact 10:74

    Article  PubMed  PubMed Central  Google Scholar 

  52. Sharon N (2006) Carbohydrates as future anti-adhesion drugs for infectious diseases. Biochim Biophys Acta 1760:527–537

    Article  CAS  PubMed  Google Scholar 

  53. Sheppard JD, Jumarie C, Cooper DG, Laprade R (1991) Ionic channels induced by surfactin in planar bilayer membranes. Biochim Biophys Acta 1064:13–23

    Article  CAS  PubMed  Google Scholar 

  54. Spanò A, Gugliandolo C, Lentini V, Maugeri TL, Anzelmo G, Poli A, Nicolaus B (2013) A novel EPS-producing strain of Bacillus licheniformis isolated from a shallow vent off Panarea Island (Italy). Curr Microbiol 67:21–29

    Article  PubMed  Google Scholar 

  55. Thenmozhi R, Nithyanand P, Rathna J, Pandian SK (2009) Antibiofilm activity of coral associated bacteria against different clinical M serotypes of Streptococcus pyogenes. FEMS Immunol Med Microbiol 57:284–294

    Article  CAS  PubMed  Google Scholar 

  56. Vanhooren PT, Vandamme EJ (1999) L-Fucose: occurrence, physiological role, chemical, enzymatic and microbial synthesis. J Chem Technol Biotechnol 74:479–497

    Article  CAS  Google Scholar 

  57. Wang J, Zhao X, Yang Y, Zhao A, Yang Z (2015) Characterization and bioactivities of an exopolysaccharide produced by Lactobacillus plantarum YW32. Int J Biol Macromol 74:119–126

    Article  CAS  PubMed  Google Scholar 

  58. You J, Xue X, Cao L, Lu X, Wang J, Zhang L, Zhou SV (2007) Inhibition of Vibrio biofilm formation by a marine actinomycete strain A66. Appl Microbiol Biotechnol 76:1137–1144

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Research Centre for Extreme Environments and Extremophiles, Department of Biological and Environmental Sciences, University of Messina, V.le F. Stagno d’Alcontres 31, 98166, Messina, Italy

    Antonio Spanò, Teresa L. Maugeri & Concetta Gugliandolo

  2. Department of Biomedical Sciences and Morphological and Functional Images, University of Messina, V. Consolare Valeria, 98125, Messina, Italy

    Pasqualina Laganà & Giuseppa Visalli

Authors
  1. Antonio Spanò
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  2. Pasqualina Laganà
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  3. Giuseppa Visalli
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  4. Teresa L. Maugeri
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  5. Concetta Gugliandolo
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Correspondence to Concetta Gugliandolo.

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Spanò, A., Laganà, P., Visalli, G. et al. In Vitro Antibiofilm Activity of an Exopolysaccharide from the Marine Thermophilic Bacillus licheniformis T14. Curr Microbiol 72, 518–528 (2016). https://doi.org/10.1007/s00284-015-0981-9

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  • DOI: https://doi.org/10.1007/s00284-015-0981-9

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