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Surfactin effectively inhibits Staphylococcus aureus adhesion and biofilm formation on surfaces

  • Applied microbial and cell physiology
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Abstract

Biosurfactants are amphiphilic compounds that composed of hydrophilic and hydrophobic moieties, which possess the ability of self-organizing between phases, reducing the interfacial tension, and forming aggregates such as micelles. This spontaneous process results in significant changes in surface properties that directly influence the adherence of microorganisms. In this study, the ability of surfactin, a biosurfactant produced by Bacillus subtilis in reducing adhesion and disrupting the presence of biofilm of Staphylococcus aureus (S. aureus) on several surfaces, was investigated. Significant biofilm removal was observed on glass, polystyrene, and stainless steel surfaces. Furthermore, we explored the probable mechanism about how surfactin affected S. aureus biofilm formation. Based on our findings, surfactin had a significant effect on the polysaccharides production and especially decreased the percentage of alkali-soluble polysaccharide in biofilms. It also down-regulated the expression of icaA and icaD significantly, which are necessary for the important constituents to take shape of staphylococcal biofilm. In addition, it was found that the lipopeptide affected the quorum sensing (QS) system in S. aureus through regulating the auto inducer 2 (AI-2) activity, which has been reported to be negative for biofilm formation in S. aureus. These above properties could be applied in developing surfactin as a potential pre-coating agent on material surfaces to prevent S. aureus biofilm formation.

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References

  • Araujo LVD, Guimarães CR, Marquita RLDS, Santiago VMJ, Souza MPD, Nitschke M, Freire DMG (2016) Rhamnolipid and surfactin: anti-adhesion/antibiofilm and antimicrobial effects. Food Control 63:171–178

    Article  CAS  Google Scholar 

  • Arima K, Kakinuma A, Tamura G (1968) Surfactin, a crystalline peptidelipid surfactant produced by Bacillus subtilis: isolation, characterization and its inhibition of fibrin clot formation. BIOCHEM BIOPH RES CO 31(3):488–494

    Article  CAS  Google Scholar 

  • Banat IM, Franzetti A, Gandolfi I, Bestetti G, Martinotti MG, Fracchia L, Smyth TJ, Marchant R (2010) Microbial biosurfactants production, applications and future potential. APPL MICROBIOL BIOT 87(2):427–444

    Article  CAS  Google Scholar 

  • Chaieb K, Kouidhi B, Jrah H, Mahdouani K, Bakhrouf A (2011) Antibacterial activity of Thymoquinone, an active principle of Nigella sativa and its potency to prevent bacterial biofilm formation. BMC Complem Altern M 11(1):1–6

  • Chen WC, Juang RS, Wei YH (2015) Applications of a lipopeptide biosurfactant, surfactin, produced by microorganisms. Biochem Eng J 103:158–169

    Article  CAS  Google Scholar 

  • Ciccio PD, Vergara A, Festino AR, Paludi D, Zanardi E, Ghidini S, Ianieri A (2015) Biofilm formation by Staphylococcus aureus on food contact surfaces: relationship with temperature and cell surface hydrophobicity. Food Control 50:930–936

    Article  CAS  Google Scholar 

  • Conlon KM, Humphreys H, O'Gara JP (2002) icaR encodes a transcriptional repressor involved in environmental regulation of ica operon expression and biofilm formation in Staphylococcus epidermidis. J Bacteriol 184(16):4400–4408

  • Cramton SE, Gerke C, Schnell NF, Nichols WW, Götz F (1999) The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun 67(10):5427–5433

  • Cue D, Lei MG, Lee CY (2013) Activation of sarX by Rbf is required for biofilm formation and icaADBC expression in Staphylococcus aureus. J Bacteriol 195(7):1515–1524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Souza EL, Meira QG, De MBI, Athayde AJ (2014) Biofilm formation by Staphylococcus aureus from food contact surfaces in a meat-based broth and sensitivity to sanitizers. Braz J Microbiol 45(1):67–75

    Article  PubMed  PubMed Central  Google Scholar 

  • Dobinsky S, Kiel K, Rohde H, Bartscht K, Knobloch JK, Horstkotte MA, Mack D (2003) Glucose-related dissociation between icaADBC transcription and biofilm expression by Staphylococcus epidermidis: evidence for an additional factor required for polysaccharide intercellular adhesin synthesis. J Bacteriol 185(9):2879–2886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durham-Colleran MW, Verhoeven AB, Hoek MLV (2010) Francisella novicida forms in vitro biofilms mediated by an orphan response regulator. Microb Ecol 59(3):457–465

    Article  PubMed  Google Scholar 

  • Fluckiger U, Ulrich M, Steinhuber A, Döring G, Mack D, Landmann R, Goerke C, Wolz C (2005) Biofilm formation, icaADBC transcription, and polysaccharide intercellular adhesin synthesis by staphylococci in a device-related infection model. Infect Immun 73(3):1811–1819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gomes MZDV, Nitschke M (2012) Evaluation of rhamnolipid and surfactin to reduce the adhesion and remove biofilms of individual and mixed cultures of food pathogenic bacteria. Food Control 25(2):441–447

    Article  CAS  Google Scholar 

  • Götz F (2002) Staphylococcus and biofilms. Mol Microbiol 43(6):1367–1378

    Article  PubMed  Google Scholar 

  • Hamme JDV, Singh A, Ward OP (2006) Physiological aspects : part 1 in a series of papers devoted to surfactants in microbiology and biotechnology. Biotechnol Adv 24(6):604–620

    Article  CAS  PubMed  Google Scholar 

  • Husain F (2014) Antibacterial and antibiofilm activity of some essential oils and compounds against clinical strains of Staphylococcus aureus. Med Phys 19(5):1307–1310

    Google Scholar 

  • Ju X, Li J, Zhu M, Lu Z, Lv F, Zhu X et al (2018) Effect of the luxs gene on biofilm formation and antibiotic resistance by Salmonella serovar Dublin. Food Res Int 107:385–393

  • Kadariya J, Smith TC, Thapaliya D (2014) Staphylococcus aureus and staphylococcal food-borne disease: an ongoing challenge in public health. Biomed Res Int 2014(2014):1–9

    Article  Google Scholar 

  • Koo H, Hayacibara MF, Schobel BD, Cury JA, Rosalen PL, Park YK, Vaccasmith AM, Bowen WH (2003) Inhibition of Streptococcus mutans biofilm accumulation and polysaccharide production by apigenin and tt-farnesol. J Antimicrob Chemoth 52(5):782–789

    Article  CAS  Google Scholar 

  • Lister JL, Horswill AR (2014) Staphylococcus aureus biofilms: recent developments in biofilm dispersal. FRONT CELL INFECT MI 4(4):178

    Google Scholar 

  • Ma R, Qiu S, Qiu J, Sun H, Xue T, Gang C, Sun B (2017) AI-2 quorum sensing negatively regulates rbf expression and biofilm formation in Staphylococcus aureus. Int J Med Microbiol 307(4–5):257–267

    Article  CAS  PubMed  Google Scholar 

  • Mack D, Becker P, Chatterjee I, Dobinsky S, Knobloch JK, Peters G, Rohde H, Herrmann M (2004) Mechanisms of biofilm formation in Staphylococcus epidermidis and Staphylococcus aureus: functional molecules, regulatory circuits, and adaptive responses. IJMM 294(2-3):203–212

    CAS  PubMed  Google Scholar 

  • Mattosgraner RO, Smith DJ, King WF, Mayer MPA (2000) Water-insoluble Glucan synthesis by mutans streptococcal strains correlates with caries incidence in 12- to 30-month-old children. J Dent Res 79(6):1371–1377

    Article  CAS  Google Scholar 

  • Mclandsborough L, Rodriguez A, Pérez-Conesa D, Weiss J (2006) Biofilms: at the interface between biophysics and microbiology. FOOD BIOPHYS 1(2):94–114

    Article  Google Scholar 

  • Monte J, Abreu AC, Borges A, Simões LC, Simões M (2014) Antimicrobial activity of selected phytochemicals against Escherichia coli and Staphylococcus aureus and their biofilms. PATHOGENS 3(2):473–498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nd MJ, Toguchi A, Harshey RM (2001) Salmonella enterica serovar typhimurium swarming mutants with altered biofilm-forming abilities: surfactin inhibits biofilm formation. J Bacteriol 183(20):5848

    Article  Google Scholar 

  • Nitschke M, Aracjo LV, Costa SGVAO, Pires RC, Zeraik AE, Fernandes ACLB, Freire DMG, Contiero J (2009) Surfactin reduces the adhesion of food-borne pathogenic bacteria to solid surfaces. Lett Appl Microbiol 49(2):241–247

    Article  CAS  PubMed  Google Scholar 

  • Peypoux F, Bonmatin JM, Wallach J (1999) Recent trends in the biochemistry of surfactin. APPL MICROBIOL BIOT 51(5):553–563

    Article  CAS  Google Scholar 

  • Rohde H, Knobloch JK, Horstkotte MA, Mack D (2001) Correlation of Staphylococcus aureus icaADBC genotype and biofilm expression phenotype. J Clin Microbiol 39(12):4595–4596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rohde H, Burandt EC, Siemssen N, Frommelt L, Burdelski C, Wurster S, Scherpe S, Davies AP, Harris LG, Horstkotte MA (2007) Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis and Staphylococcus aureus isolated from prosthetic hip and knee joint infections. BIOMATERIALS 28(9):1711–1720

    Article  CAS  PubMed  Google Scholar 

  • Ruiz LM, Valenzuela S, Castro M, Gonzalez A, Frezza M, Soulère L, Rohwerder T, Queneau Y, Doutheau A, Sand W (2008) AHL communication is a widespread phenomenon in biomining bacteria and seems to be involved in mineral-adhesion efficiency. HYDROMETALLURGY 94(1–4):133–137

    Article  CAS  Google Scholar 

  • Sen R (2010) Surfactin: biosynthesis, genetics and potential applications. Adv Exp Med Biol 672(672):316–323

    Article  CAS  PubMed  Google Scholar 

  • Seydlová G, Svobodová J (2008) Review of surfactin chemical properties and the potential biomedical applications. CENT EUR J MED 3(2):123–133

    Google Scholar 

  • Shaligram NS, Singhal RS (2010) Surfactin - a review on biosynthesis, fermentation, purification and applications. FOOD TECHNOL BIOTECH 48(2):119–134

    CAS  Google Scholar 

  • Simões M, Simões LC, Vieira MJ (2010) A review of current and emergent biofilm control strategies. LWT-FOOD SCI TECHNOL 43(4):573–583

    Article  CAS  Google Scholar 

  • Sun Z, He X, Brancaccio VF, Yuan J, Riedel CU (2014) Bifidobacteria exhibit LuxS-dependent autoinducer 2 activity and biofilm formation. PLOS ONE 9(2):e88260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Treter J, Bonatto F, Krug C, Soares GV, Baumvol IJR, Macedo AJ (2014) Washing-resistant surfactant coated surface is able to inhibit pathogenic bacteria adhesion. Appl Surf Sci 303(303):147–154

    Article  CAS  Google Scholar 

  • Verheyen CC, Dhert WJ, de BlieckHogervorst JM, Tj VDR, Petit PL, De GK (1993) Adherence to a metal, polymer and composite by Staphylococcus aureus and Staphylococcus epidermidis. BIOMATERIALS 14(5):383–391

    Article  CAS  PubMed  Google Scholar 

  • Vu B, Chen M, Crawford RJ, Ivanova EP (2009) Bacterial extracellular polysaccharides involved in biofilm formation. MOLECULES 14(7):2535–2554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Lu Z, Wu H, Lv F (2009) Study on the antibiotic activity of microcapsule curcumin against foodborne pathogens. Int J Food Microbiol 136(1):71–74

    Article  CAS  PubMed  Google Scholar 

  • Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21(21):319

    Article  CAS  PubMed  Google Scholar 

  • Xi X, Wei X, Wang Y, Chu Q, Xiao J (2010) Determination of tea polysaccharides in camellia sinensis by a modified phenol-sulfuric acid method. ARCH BIOL SCI 62(3):669–676

    Article  Google Scholar 

  • Yu D, Zhao L, Xue T, Sun B (2012) Staphylococcus aureus autoinducer-2 quorum sensing decreases biofilm formation in an icaR-dependent manner. BMC Microbiol 12(1):288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Y, Weiss EC, Otto M, Fey PD, Smeltzer MS, Somerville GA (2007) Staphylococcus aureus biofilm metabolism and the influence of arginine on polysaccharide intercellular adhesin synthesis, biofilm formation, and pathogenesis. Infect Immun 75(9):4219–4226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ziebuhr W, Mühldorfer I, Schäfer KP (2001) Staphylococcus aureus and Staphylococcus epidermidis: emerging pathogens in nosocomial infections. Contrib Microbiol 8(8):102–107

    Article  CAS  PubMed  Google Scholar 

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Funding

This study was funded by the National Natural Science Foundation of China (No.31571887), Agricultural Innovation foundation of Jiangsu Province (CX 16-1058).

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Correspondence to Zhaoxin Lu.

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Liu, J., Li, W., Zhu, X. et al. Surfactin effectively inhibits Staphylococcus aureus adhesion and biofilm formation on surfaces. Appl Microbiol Biotechnol 103, 4565–4574 (2019). https://doi.org/10.1007/s00253-019-09808-w

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