Skip to main content
PMC home page
Food Science and Biotechnology logoLink to Food Science and Biotechnology
. 2016 Apr 30;25(2):643–648. doi: 10.1007/s10068-016-0090-y

Biofilm formation and cell surface properties of Staphylococcus aureus isolates from various sources

Bo-Ram Kim 1, Young-Min Bae 1, Jin-Ha Hwang 1, Sun-Young Lee 1,✉
PMCID: PMC6049189  PMID: 30263318

Abstract

This study investigated biofilm formation, cell surface hydrophobicity, colony spreading, and slime production for 112 Staphylococcus aureus strains isolated from various sources (leaf vegetables, pea leaf, perilla leaf, Kim-bab, person, and animal). When biofilm formation was classified by origin, S. aureus isolated from animal origin showed a significantly higher level of biofilm formation than others (p≤0.05). When S. aureus groups with different levels of biofilm formation (very strong, strong, moderate, and weak) were evaluated for the correlation with cell surface properties, there was a positive correlation between biofilm formation and hydrophobicity (r=0.926). Biofilm formation and colony spreading on tryptic soy broth (without dextrose) also showed positive correlation (r=0.863). In contrast, biofilm formation and slime production were negatively correlated (r=−0.973). Based on these results, the biofilm forming ability of S. aureus differs depending on their origin and might be affected by cell surface properties such as cell surface hydrophobicity.

Keywords: Staphylococcus aureus, biofilm, cell surface properties, hydrophobicity, correlation

References

  • 1.Kaito C, Sekimizu K. Colony spreading in Staphylococcus aureus. J. Bacteriol. 2007;189:2553–2557. doi: 10.1128/JB.01635-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Jamalia H, Paydar M, Radmehr B, Ismail S, Dadrasnia A. Prevalence and antimicrobial resistance of Staphylococcus aureus isolated from raw milk and dairy products. Food Control. 2015;54:383–388. doi: 10.1016/j.foodcont.2015.02.013. [DOI] [Google Scholar]
  • 3.Enright MC. The evolution of resistant pathogen-the case of MRSA. Curr. Opin. Pharmacol. 2003;3:474–479. doi: 10.1016/S1471-4892(03)00109-7. [DOI] [PubMed] [Google Scholar]
  • 4.Gorman R, Bloomfield S, Adley CC. A study of cross-contamination of foodborne pathogens in the domestic kitchen in the Republic of Ireland. Int. J. Food Microbiol. 2002;76:143–150. doi: 10.1016/S0168-1605(02)00028-4. [DOI] [PubMed] [Google Scholar]
  • 5.Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. Microbial biofilms. Annu. Rev. Microbiol. 1995;49:711–745. doi: 10.1146/annurev.mi.49.100195.003431. [DOI] [PubMed] [Google Scholar]
  • 6.Xu H, Lee HY, Ahn J. Characteristics of biofilm formation by selected foodborne pathogens. J. Food Safety. 2011;31:91–97. doi: 10.1111/j.1745-4565.2010.00271.x. [DOI] [Google Scholar]
  • 7.Pagedar A, Singh J, Batish VK. Surface hydrophobicity, nutritional contents affect Staphylococcus aureus biofilms and temperature influences its survival in preformed biofilms. J. Basic Microb. 2010;50:S98–S106. doi: 10.1002/jobm.201000034. [DOI] [PubMed] [Google Scholar]
  • 8.Götz F. Staphylococcus and biofilms. Mol. Microbiol. 2002;43:1367–1378. doi: 10.1046/j.1365-2958.2002.02827.x. [DOI] [PubMed] [Google Scholar]
  • 9.Vatsos IN, Thompson KD, Adams A. Adhesion of the fish pathogen Flavobacterium psychrophilum to unfertilized eggs of rainbow trout (Oncorhynchus mykiss) and n-hexadecane. Lett. Appl. Microbiol. 2001;33:178–182. doi: 10.1046/j.1472-765x.2001.00980.x. [DOI] [PubMed] [Google Scholar]
  • 10.Sibbald MJJB, Ziebandt AK, Engelmann S, Hecker M, de Jong A, Harmsen HJM, Raangs GC, Stokroos I, Arends JP, Dubois JYF, van Dijl JM. Mapping the pathways to staphylococcal pathogenesis by comparative secretomics. Microbiol. Mol. Biol. R. 2006;70:755–788. doi: 10.1128/MMBR.00008-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Gallardo-Moreno AM, González-Martín ML, Pérez-Giraldo C, Bruque JM, Gómez-García AC. Serum as a factor influencing adhesion of Enterococcus faecalis to glass and silicone. Appl. Environ. Microb. 2002;68:5784–5787. doi: 10.1128/AEM.68.11.5784-5787.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Howard ST, Rhoades E, Recht J, Pang X, Alsup A, Kolter R, Lyons CR, Byrd TF. Spontaneous reversion of Mycobacterium abscessus from a smooth to a rough morphotype is associated with reduced expression of glycopeptidolipid and reacquisition of an invasive phenotype. Microbiology. 2006;152:1581–1590. doi: 10.1099/mic.0.28625-0. [DOI] [PubMed] [Google Scholar]
  • 13.Deighton MA, Capstick J, Borland R. A study of phenotypic variation of Staphylococcus epidermidis using Congo red agar. Epidemiol. Infect. 1992;109:423–432. doi: 10.1017/S095026880005041X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Christensen GD, Simpson WA, Bisno AL, Beachey EH. Adherence of slimeproducing strains of Staphylococcus epidermidis to smooth surfaces. Infect. Immun. 1982;37:318–326. doi: 10.1128/iai.37.1.318-326.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Arciola CR, Campoccia D, Montanaro L. Detection of biofilm-forming strains of Staphylococcus epidermidis and S. aureus. Expert Rev. Mol. Diagn. 2002;2:478–484. doi: 10.1586/14737159.2.5.478. [DOI] [PubMed] [Google Scholar]
  • 16.Djordjevic D, Wiedmann M, Mclandsborough LA. Microtitier plates assay for assessment of Listeria monocytogenes biofilm formation. Appl. Environ. Microb. 2002;68:2950–2958. doi: 10.1128/AEM.68.6.2950-2958.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Goulter RM, Gentle IR, Dykes GA. Characterisation of curli production, cell surface hydrophobicity, autoaggregation and attachment behavior of Escherichia coli O157. Curr. Microbiol. 2010;61:157–162. doi: 10.1007/s00284-010-9589-2. [DOI] [PubMed] [Google Scholar]
  • 18.Freeman DJ, Falkiner FR, Keane CT. New method for detecting slime production by coagulase negative staphylococci. J. Clin. Pathol. 1989;42:872–874. doi: 10.1136/jcp.42.8.872. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Oliveira A C, Mde L. Comparison of methods for the detection of biofilm production in coagulase-negative staphylococci. BMC Res. Notes. 2010;3:260. doi: 10.1186/1756-0500-3-260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Stepanoviæ S, Vukoviæ D, Hola V, Di Bonaventura G, Djukiæ S, Cirkoviæ I, Ruzicka F. Quantification of biofilm in microtiter plates: Overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS. 2007;115:891–899. doi: 10.1111/j.1600-0463.2007.apm_630.x. [DOI] [PubMed] [Google Scholar]
  • 21.Cha JO, Park YK, Lee YS, Chung GT. In vitro biofilm formation and bacterial activities of methicillin-resistant Staphylococcus aureus clones prevalent in Korea. Diagn. Micr. Infec. Dis. 2011;70:112–118. doi: 10.1016/j.diagmicrobio.2010.11.018. [DOI] [PubMed] [Google Scholar]
  • 22.Takahashi H, Miya S, Igarashi K, Suda T, Kuramoto S, Kimura B. Biofilm formation ability of Listeria monocytogenes isolates from raw ready-to-eat seafood. J. Food Protect. 2009;72:1476–1480. doi: 10.4315/0362-028x-72.7.1476. [DOI] [PubMed] [Google Scholar]
  • 23.Nilsson RE, Ross T, Bowman JP. Variability in biofilm production by Listeria monocytogenes correlated to strain origin and growth conditions. Int. J. Food Microbiol. 2011;150:14–24. doi: 10.1016/j.ijfoodmicro.2011.07.012. [DOI] [PubMed] [Google Scholar]
  • 24.Mohamed JA, Huang W, Nallapareddy SR, Teng F, Murray BE. Influence of origin of isolates, especially endocarditis isolates, and various genes on biofilm formation by Enterococcus faecalis. Infect. Immun. 2004;72:3658–3663. doi: 10.1128/IAI.72.6.3658-3663.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Takahashi H, Suda T, Tanaka Y, Kimura B. Cellular hydrophobicity of Listeria monocytogenes involves initial attachment and biofilm formation on the surface of polyvinyl chloride. Lett. Appl. Microbiol. 2010;50:618–625. doi: 10.1111/j.1472-765X.2010.02842.x. [DOI] [PubMed] [Google Scholar]
  • 26.Pasmore M, Todd P, Smith S, Baker D, Silverstein J, Coons D, Bowman CN. Effects of ultrafiltration membrane surface properties on Pseudomonas aeruginosa biofilm initiation for the purpose of reducing biofouling. J. Membrane Sci. 2001;30:15–32. doi: 10.1016/S0376-7388(01)00468-9. [DOI] [Google Scholar]
  • 27.Ukuku DO, Fett WF. Relationship of cell surface charge and hydrophobicity to strength of attachment of bacteria to cantaloupe rind. J. Food Protect. 2002;65:1093–1099. doi: 10.4315/0362-028x-65.7.1093. [DOI] [PubMed] [Google Scholar]
  • 28.Auger S, Ramarao N, Faille C, Fouet A, Aymerich S, Gohar M. Biofilm formation and cell surface properties among pathogenic and nonpathogenic strains of the Bacillus cereus group. Appl. Environ. Microb. 2009;75:6616–6618. doi: 10.1128/AEM.00155-09. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Flint SH, Brooks JD, Bremer PJ. The influence of cell surface properties of thermophilic streptococci on attachment to stainless steel. J. Appl. Microbiol. 1997;93:508–517. doi: 10.1046/j.1365-2672.1997.00264.x. [DOI] [PubMed] [Google Scholar]
  • 30.O’Toole GA, Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 1998;30:295–304. doi: 10.1046/j.1365-2958.1998.01062.x. [DOI] [PubMed] [Google Scholar]
  • 31.Agustí G, Astola O, Rodríguez-Güell E, Julián E, Luquin M. Surface spreading motility shown by a group of phylogenetically related, rapidly growing pigmented mycobacteria suggests that motility is a common property of mycobacterial species but is restricted to smooth colonies. J. Bacteriol. 2008;190:6894–6902. doi: 10.1128/JB.00572-08. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Ueda T, Kaico C, Omae Y, Sekimizu K. Sugar-responsive gene expression and the agr system are required for colony spreading in Staphylococcus aureus. Microb. Pathogenesis. 2011;51:178–185. doi: 10.1016/j.micpath.2011.04.003. [DOI] [PubMed] [Google Scholar]
  • 33.Tojo M, Yamashita N, Goldmann DA, Pier GB. Isolation and characterization of a capsular polysaccharide adhesion from Staphylococcus epidermidis. J. Infect. Dis. 1988;157:713–722. doi: 10.1093/infdis/157.4.713. [DOI] [PubMed] [Google Scholar]
  • 34.Arciola CR, Baldassarri L, Montanaro L. Presence of icaA and icaD genes slime production in a collection of staphylococcal strains from catheter-associated infections. J. Clin. Microbiol. 2001;39:2151–2156. doi: 10.1128/JCM.39.6.2151-2156.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Oliveria M, Bexiga R, Nunes SF, Carneiro C, Cavaco LM, Bernardo F, Vilela CL. Biofilm-forming ability profiling of Staphylococcus aureus and Staphylococcus epidermidis mastitis isolates. Vet. Microbiol. 2006;118:133–140. doi: 10.1016/j.vetmic.2006.07.008. [DOI] [PubMed] [Google Scholar]

Articles from Food Science and Biotechnology are provided here courtesy of Springer

RESOURCES