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

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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.

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References

  1. Kaito C, Sekimizu K. Colony spreading in Staphylococcus aureus. J. Bacteriol. 189: 2553–2557 (2007)

    Article  CAS  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 54: 383–388 (2015)

    Article  Google Scholar 

  3. Enright MC. The evolution of resistant pathogen-the case of MRSA. Curr. Opin. Pharmacol. 3: 474–479 (2003)

    Article  CAS  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. 76: 143–150 (2002)

    Article  Google Scholar 

  5. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. Microbial biofilms. Annu. Rev. Microbiol. 49: 711–745 (1995)

    Article  CAS  Google Scholar 

  6. Xu H, Lee HY, Ahn J. Characteristics of biofilm formation by selected foodborne pathogens. J. Food Safety 31: 91–97 (2011)

    Article  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. 50: S98–S106 (2010)

    Article  Google Scholar 

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

    Article  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. 33: 178–182 (2001)

    Article  CAS  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. 70: 755–788 (2006)

    Article  CAS  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. 68: 5784–5787 (2002)

    Article  CAS  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 152: 1581–1590 (2006)

    Article  CAS  Google Scholar 

  13. Deighton MA, Capstick J, Borland R. A study of phenotypic variation of Staphylococcus epidermidis using Congo red agar. Epidemiol. Infect. 109: 423–432 (1992)

    Article  CAS  Google Scholar 

  14. Christensen GD, Simpson WA, Bisno AL, Beachey EH. Adherence of slimeproducing strains of Staphylococcus epidermidis to smooth surfaces. Infect. Immun. 37: 318–326 (1982)

    CAS  Google Scholar 

  15. Arciola CR, Campoccia D, Montanaro L. Detection of biofilm-forming strains of Staphylococcus epidermidis and S. aureus. Expert Rev. Mol. Diagn. 2: 478–484 (2002)

    Article  CAS  Google Scholar 

  16. Djordjevic D, Wiedmann M, Mclandsborough LA. Microtitier plates assay for assessment of Listeria monocytogenes biofilm formation. Appl. Environ. Microb. 68: 2950–2958 (2002)

    Article  CAS  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. 61: 157–162 (2010)

    Article  CAS  Google Scholar 

  18. Freeman DJ, Falkiner FR, Keane CT. New method for detecting slime production by coagulase negative staphylococci. J. Clin. Pathol. 42: 872–874 (1989)

    Article  CAS  Google Scholar 

  19. Oliveira A, Cunha Mde L. Comparison of methods for the detection of biofilm production in coagulase-negative staphylococci. BMC Res. Notes 3: 260 (2010)

    Article  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 115: 891–899 (2007)

    Article  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. 70: 112–118 (2011)

    Article  CAS  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. 72: 1476–1480 (2009)

    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. 150: 14–24 (2011)

    Article  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. 72: 3658–3663 (2004)

    Article  CAS  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. 50: 618–625 (2010)

    Article  CAS  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. 30: 15–32 (2001)

    Article  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. 65: 1093–1099 (2002)

    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. 75: 6616–6618 (2009)

    Article  CAS  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. 93: 508–517 (1997)

    Article  Google Scholar 

  30. O’Toole GA. Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30: 295–304 (1998)

    Article  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. 190: 6894–6902 (2008)

    Article  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 51: 178–185 (2011)

    Article  CAS  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. 157: 713–722 (1988)

    Article  CAS  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. 39: 2151–2156 (2001)

    Article  CAS  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. 118: 133–140 (2006)

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Food Science and Technology, Chung-Ang University, Anseong, Gyeonggi, 17546, Korea

    Bo-Ram Kim, Young-Min Bae, Jin-Ha Hwang & Sun-Young Lee

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  1. Bo-Ram Kim
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  2. Young-Min Bae
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  3. Jin-Ha Hwang
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  4. Sun-Young Lee
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Correspondence to Sun-Young Lee.

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Kim, BR., Bae, YM., Hwang, JH. et al. Biofilm formation and cell surface properties of Staphylococcus aureus isolates from various sources. Food Sci Biotechnol 25, 643–648 (2016). https://doi.org/10.1007/s10068-016-0090-y

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  • DOI: https://doi.org/10.1007/s10068-016-0090-y

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