Advertisement

Antonie van Leeuwenhoek

, Volume 109, Issue 10, pp 1375–1388 | Cite as

Lipopeptides from Bacillus subtilis AC7 inhibit adhesion and biofilm formation of Candida albicans on silicone

  • Chiara Ceresa
  • Maurizio Rinaldi
  • Valeria Chiono
  • Irene Carmagnola
  • Gianna Allegrone
  • Letizia FracchiaEmail author
Original Paper

Abstract

Candida albicans is the major fungus that colonises medical implants, causing device-associated infections with high mortality. Antagonistic bacterial products with interesting biological properties, such as biosurfactants, have recently been considered for biofilm prevention. This study investigated the activity of lipopeptide biosurfactant produced by Bacillus subtilis AC7 (AC7 BS) against adhesion and biofilm formation of C. albicans on medical-grade silicone elastomeric disks (SEDs). Chemical analysis, stability, surface activities of AC7 BS crude extract and physicochemical characterisation of the coated silicone disk surfaces were also carried out. AC7 BS showed a good reduction of water surface tension, low critical micelle concentration, good emulsification activity, thermal resistance and pH stability. Co-incubation with 2 mg ml−1 AC7 BS significantly reduced adhesion and biofilm formation of three C. albicans strains on SEDs in a range of 67–69 % and of 56–57 %, respectively. On pre-coated SEDs, fungal adhesion and biofilm formation were reduced by 57–62 % and 46–47 %, respectively. Additionally, AC7 BS did not inhibit viability of C. albicans strains in both planktonic and sessile form. Chemical analysis of the crude extract revealed the presence of two families of lipopeptides, principally surfactin and a lower percentage of fengycin. The evaluation of surface wettability indicated that AC7 BS coating of SEDs surface was successful although uneven. AC7 BS significantly prohibits the initial deposition of C. albicans and slows biofilm growth, suggesting a potential role of biosurfactant coatings for preventing fungal infection associated with silicone medical devices.

Keywords

Anti-adhesion Biofilm Medical device Lipopeptide biosurfactant Coating Candida albicans 

Notes

Acknowledgments

This work was partially funded by Regione Piemonte Grant POR-FESR Asse I—AGROBIOCAT Project.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Almirante B, Rodrıguez D, Park BJ et al (2005) Epidemiology and predictors of mortality in cases of Candida bloodstream infection: results from population-based surveillance, Barcelona, Spain, from 2002 to 2003. J Clin Microbiol 43:1829–1835CrossRefPubMedPubMedCentralGoogle Scholar
  2. Amani H, Sarrafzadeh MH, Haghighi M, Mehrnia MR (2010) Comparative study of biosurfactant producing bacteria in MEOR applications. J Pet Sci Eng 75:209–214CrossRefGoogle Scholar
  3. Banat IM, Franzetti A, Gandolfi I et al (2010) Microbial biosurfactants production, applications and future potential. Appl Microbiol Biotechnol 87:427–444. doi: 10.1007/s00253-010-2589-0 CrossRefPubMedGoogle Scholar
  4. Biniarz P, Baranowska G, Feder-Kubis J, Krasowska A (2015) The lipopeptides pseudofactin II and surfactin effectively decrease Candida albicans adhesion and hydrophobicity. Antonie Van Leeuwenhoek 108:343–353. doi: 10.1007/s10482-015-0486-3 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Busscher HJ, van Hoogmoed CG, Geertsema-Doornbusch GI, van der Kuijl-Booij M, van der Mei HC (1997) Streptococcus thermophilus and its biosurfactants inhibit adhesion by Candida spp. on silicone rubber. Appl Environ Microbiol 63:3810–3817PubMedPubMedCentralGoogle Scholar
  6. Cameotra SS, Makkar RS (2004) Recent applications of biosurfactants as biological and immunological molecules. Curr Opin Microbiol 7:262–266CrossRefPubMedGoogle Scholar
  7. Ceresa C, Tessarolo F, Caola I (2015) Inhibition of Candida albicans adhesion on medical-grade silicone by a Lactobacillus-derived biosurfactant. J Appl Microbiol 118:1116–1125. doi: 10.1111/jam.12760 CrossRefPubMedGoogle Scholar
  8. Chandra J, Mukherjee PK, Ghannoum MA (2008) In vitro growth and analysis of Candida biofilms. Nat Protoc 3:1909–1924. doi: 10.1038/nprot.2008.192 CrossRefPubMedGoogle Scholar
  9. Cochis A, Fracchia L, Martinotti MG, Rimondini L (2012) Biosurfactants prevent in vitro Candida albicans biofilm formation on resins and silicon materials for prosthetic devices. Oral Surg Oral Med Oral Pathol Oral Radiol 113:755–761. doi: 10.1016/j.oooo.2011.11.004 CrossRefPubMedGoogle Scholar
  10. Comoglio F, Fracchia L, Rinaldi M (2013) Bayesian inference from count data using discrete uniform priors. PLoS One. doi: 10.1371/journal.pone.0074388 PubMedPubMedCentralGoogle Scholar
  11. Crump JA, Collignon PJ (2000) Intravascular Catheter-Associated Infections. Eur J Clin Microbiol Infect Dis 19:1–8CrossRefPubMedGoogle Scholar
  12. de Sainte CP (2009) Degradation of PEO in the solid state: a theoretical kinetic model. Macromolecules 42:3469–3482CrossRefGoogle Scholar
  13. Elazzazy AM, Abdelmoneim TS, Almaghrabi OA (2015) Isolation and characterization of biosurfactant production under extreme environmental conditions by alkali-halo-thermophilic bacteria from Saudi Arabia. Saudi J Biol Sci 22:466–475CrossRefPubMedGoogle Scholar
  14. Espinel-Ingroff A, Canton E, Martin-Mazuelos E, Pemán J (2009) Pharmacotherapy of Candida infections with echinocandins. Clin Med Insights Ther 1:889–897Google Scholar
  15. Falagas ME, Makris GC (2009) Probiotic bacteria and biosurfactants for nosocomial infection control: a hypothesis. J Hosp Infect 71:301–306. doi: 10.1016/j.jhin.2008.12.008 CrossRefPubMedGoogle Scholar
  16. Fanning S, Mitchell AP (2012) Fungal biofilms. PLoS Pathog. doi: 10.1371/journal.ppat.1002585 Google Scholar
  17. Ferreira AM, Carmagnola I, Chiono V et al (2013) Surface modification of poly(dimethylsiloxane) by two-step plasma treatment for further grafting with chitosan–Rose Bengal photosensitizer. Surf Coat Technol 223:92–97CrossRefGoogle Scholar
  18. Fracchia L, Cavallo M, Allegrone G, Martinotti MG (2010) A Lactobacillus-derived biosurfactant inhibits biofilm formation of human pathogenic Candida albicans biofilm producers. In: Méndez-Vilas A (ed) Current research, technology and education topics in applied microbiology and microbial biotechnology. Formatex Research Center, Badajoz, pp 827–837Google Scholar
  19. Fracchia L, Banat JJ, Cavallo M et al (2015) Potential therapeutic applications of microbial surface-active compounds. AIMS Bioeng 2:144–162CrossRefGoogle Scholar
  20. Franzetti A, Gandolfi I, Raimondi C et al (2012) Environmental fate, toxicity, characteristics and potential applications of novel bioemulsifiers produced by Variovorax paradoxus 7bCT5. Bioresour Technol 108:245–251. doi: 10.1016/j.biortech.2012.01.005 CrossRefPubMedGoogle Scholar
  21. Ghojavand H, Vahabzadeh F, Roayaei E, Shahraki AK (2008) Production and properties of a biosurfactant obtained from a member of the Bacillus subtilis group (PTCC 1696). J Colloid Interface Sci 324:17–26. doi: 10.1016/j.jcis.2008.05.001 CrossRefGoogle Scholar
  22. Goldberg SP, Baddley JW, Aaron MF, Pappas PG, Holman WL (2000) Fungal infections in ventricular assist devices. ASAIO J 46:S37–S40CrossRefPubMedGoogle Scholar
  23. Guery B, Arendrup M, Auzinger G et al (2009) Management of invasive candidiasis and candidemia in adult non-neutropenic intensive care unit patients: part I. Epidemiology and diagnosis. Intensive Care Med 35:55–62. doi: 10.1007/s00134-008-1338-7 CrossRefPubMedGoogle Scholar
  24. Hawser SP, Douglas LJ (1994) Biofilm formation by Candida species on the surface of catheter materials in vitro. Infect Immun 62:915–921PubMedPubMedCentralGoogle Scholar
  25. Hegstad K, Langsrud S, Lunestad BT, Scheie AA, Sunde M, Yazdankhah SP (2010) Does the wide use of quaternary ammonium compounds enhance the selection and spread of antimicrobial resistance and thus threaten our health? Microb Drug Resist 16:91–104. doi: 10.1089/mdr.2009.0120 CrossRefPubMedGoogle Scholar
  26. Horn DL, Neofytos D, Anaissie EJ et al (2009) Epidemiology and outcomes of candidemia in 2019 patients: data from the prospective antifungal therapy alliance registry. Clin Infect Dis 48:1695–1703. doi: 10.1086/599039 CrossRefPubMedGoogle Scholar
  27. Janek T, Lukaszewicz M, Krasowska A (2012) Antiadhesive activity of the biosurfactant pseudofactin II secreted by the Arctic bacterium Pseudomonas fluorescens BD5. BMC Microbiol. doi: 10.1186/1471-2180-12-24 PubMedPubMedCentralGoogle Scholar
  28. Joshi S, Bharucha C, Desai A (2008) Production of biosurfactant and antifungal compound by fermented food isolate Bacillus subtilis 20B. Bioresour Technol 99:4603–4608CrossRefPubMedGoogle Scholar
  29. Kanna R, Gummadi SN, Kumar GS (2014) Production and characterization of biosurfactant by Pseudomonas putida MTCC 2467. J Biol Sci 14:436–445CrossRefGoogle Scholar
  30. Karchmer AV (2000) Infections of prosthetic valves and intravascular devices. In: Mandell G, Bennett JE, Dolin R (eds) Principles and practice of infectious diseases. Churchill Livingstone, Elsevier, Philadelphia, pp 903–917Google Scholar
  31. Kim HS, Yoon BD, Lee CH et al (1997) Production and properties of a lipopeptide biosurfactant from Bacillus subtilis C9. J Ferment Bioeng 84:41–46. doi: 10.1016/S0922-338X(97)82784-5 CrossRefGoogle Scholar
  32. Kim PI, Ryu J, Kim YH, Chi YT (2010) Production of biosurfactant lipopeptides Iturin A, fengycin and surfactin A from Bacillus subtilis CMB32 for control of Colletotrichum gloeosporioides. J Microbiol Biotechnol 20:138–145PubMedGoogle Scholar
  33. Kojic EM, Darouiche RO (2004) Candida infections on medical devices. Clin Microbiol Rev 17:255–267. doi: 10.1128/CMR.17.2.255-267.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Kullberg BJ, Verweij PE, Akova M et al (2011) European expert opinion on the management of invasive candidiasis in adults. Clin Microbiol Infect 17:1–12. doi: 10.1111/j.1469-0691.2011.03615.x CrossRefPubMedGoogle Scholar
  35. Lai CC, Wang CY, Liu WL, Huang YT, Hsueh PR (2012) Time to positivity of blood cultures of different Candida species causing fungaemia. J Med Microbiol 61:701–704. doi: 10.1099/jmm.0.038166-0 CrossRefPubMedGoogle Scholar
  36. Lazzell AL, Chaturvedi AK, Pierce CG, Prasad D, Uppuluri P, Lopez-Ribot JL (2009) Treatment and prevention of Candida albicans biofilms with caspofungin in a novel central venous catheter murine model of candidiasis. J Antimicrob Chemother 64:567–570. doi: 10.1093/jac/dkp242 CrossRefPubMedGoogle Scholar
  37. Lee SC, Yoo JS, Kim SH et al (2006) Production and characterization of lipopeptide biosurfactant from Bacillus subtilis A8–8. J Microbiol Biotechnol 16:716–723Google Scholar
  38. Maki DG, Tambyah PA (2001) Engineering out the risk for infection with urinary catheters. Emerg Infect Dis 7:342–347CrossRefPubMedPubMedCentralGoogle Scholar
  39. Mayer FL, Wilson D, Hube B (2013) Candida albicans pathogenicity mechanisms. Virulence 4:119–128. doi: 10.4161/viru.22913 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Nitschke M, Pastore GM (2006) Production and properties of a surfactant obtained from Bacillus subtilis grown on cassava wastewater. Bioresour Technol 97:336–341CrossRefPubMedGoogle Scholar
  41. Pecci Y, Rivardo F, Martinotti MG, Allegrone GJ (2010) LC/ESI-MS/MS characterisation of lipopeptide biosurfactants produced by the Bacillus licheniformis V9T14 strain. Mass Spectrom 45:772–778. doi: 10.1002/jms.1767 CrossRefGoogle Scholar
  42. Ramage G, Saville SP, Thomas DP, López-Ribot JL (2005) Candida biofilms: an update. Eukaryot Cell 4:633–638CrossRefPubMedPubMedCentralGoogle Scholar
  43. Rautela R, Singh AK, Shukla A, Cameotra SS (2014) Lipopeptides from Bacillus strain AR2 inhibits biofilm formation by Candida albicans. Antonie Van Leeuwenhoek 105:809–821CrossRefPubMedGoogle Scholar
  44. Rivardo F, Turner RJ, Allegrone G, Ceri H, Martinotti MG (2009) Anti-adhesion activity of two biosurfactants produced by Bacillus spp. prevents biofilm formation of human bacterial pathogens. Appl Microbiol Biotechnol 83:541–553. doi: 10.1007/s00253-009-1987-7 CrossRefPubMedGoogle Scholar
  45. Rivardo F, Martinotti MG, Turner RJ, Ceri H (2011) Synergistic effect of lipopeptide biosurfactant with antibiotics against Escherichia coli CFT073 biofilm. Int J Antimicrob Aging 37:324–331. doi: 10.1016/j.ijantimicag.2010.12.011 CrossRefGoogle Scholar
  46. Rodrigues LR, Teixeira JA (2010) Biomedical and therapeutic applications of biosurfactants. Adv Exp Med Biol 672:75–87CrossRefPubMedGoogle Scholar
  47. Rodrigues L, Banat IM, Teixeira J, Oliveira R (2006a) Biosurfactants: potential applications in medicine. J Antimicrob Chemother 57:609–618CrossRefPubMedGoogle Scholar
  48. Rodrigues LR, Banat IM, van der Mei HC, Teixeira JA, Oliveira R (2006b) Interference in adhesion of bacteria and yeasts isolated from explanted voice prostheses to silicone rubber by rhamnolipid biosurfactants. J Appl Microbiol 100:470–480CrossRefPubMedGoogle Scholar
  49. Rodriguez-Tudela JL, Arendrup MC, Barchiesi F et al (2008) EUCAST definitive document EDef 7.1: method for the determination of broth dilution MICs of antifungal agents for fermentative yeasts. Clin Microbiol Infect 14:398–405CrossRefGoogle Scholar
  50. Ruhnke M, Rickerts V, Cornely OA et al (2011) Diagnosis and therapy of Candida infections: joint recommendations of the German speaking mycological society and the paul-ehrlich-society for chemotherapy. Mycoses 54:279–310. doi: 10.1111/j.1439-0507.2011.02040.x CrossRefPubMedGoogle Scholar
  51. Seydlová G, Svobodová J (2008) Review of surfactin chemical properties and the potential biomedical applications. Cent Eur J Med 3:123–133Google Scholar
  52. Singh P, Cameotra SS (2004) Potential applications of microbial surfactants in biomedical sciences. Trends Biotechnol 22:142–146CrossRefPubMedGoogle Scholar
  53. Singh A, Van Hamme JD, Ward OP (2007) Surfactants in microbiology and biotechnology: part 2. Application aspects. Biotechnol Adv 25:99–121CrossRefPubMedGoogle Scholar
  54. Thompson DS, Carlisle PL, Kadosh D (2011) Coevolution of morphology and virulence in Candida species. Eukaryot Cell 10:1173–1182. doi: 10.1128/EC.05085-11 CrossRefPubMedPubMedCentralGoogle Scholar
  55. van de Veerdonk FL, Netea MG, Joosten LA, van der Meer JWM, Kullberg BJ (2010) Novel strategies for the prevention and treatment of Candida infections: the potential of immunotherapy. FEMS Microbiol Rev 34:1063–1075. doi: 10.1111/j.1574-6976.2010.00232.x CrossRefPubMedGoogle Scholar
  56. Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB (2004) Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 39:309–317CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Pharmaceutical SciencesUniversità del Piemonte Orientale “A. Avogadro”NovaraItaly
  2. 2.Department of Mechanical and Aerospace EngineeringPolitecnico di TorinoTurinItaly

Personalised recommendations