Inhibitory effect of probiotic yeast Saccharomyces cerevisiae on biofilm formation and expression of α-hemolysin and enterotoxin A genes of Staphylococcus aureus
Abstract
Background and Objectives: Staphylococcus aureus, as an opportunistic pathogen, is the cause of a variety of diseases from mild skin infections to severe invasive infections and food poisoning. Increasing antibiotic resistance in S. aureus isolates has become a major threat to public health. The use of compounds produced by probiotics can be a solution to this problem. Thus, the purpose of this study was to investigate the effect of Saccharomyces cerevisiae on some virulence factors (biofilm, α-hemolysin, and enterotoxin A) of S. aureus.
Materials and Methods: Supernatant and lysate extracts were prepared from S. cerevisiae S3 culture. Sub-MIC concentrations of both extracts were separately applied to S. aureus ATCC 29213 (methicillin-sensitive S. aureus; MSSA) and S. aureus ATCC 33591 (methicillin-resistant S. aureus; MRSA) strains. Biofilm formation of these strains was measured by microtiter plate assay and expression level of α-hemolysin and enterotoxin A genes (hla and sea, respectively) using real-time PCR technique.
Results: The supernatant extract has reduced both biofilm formation and expression of sea and hla genes, while lysate extract had only anti-biofilm effects. The MRSA strain showed more susceptibility to yeast extracts than MSSA strain in all tests.
Conclusion: The present study exhibited favorable antagonistic effects of S. cerevisiae S3, as a probiotic yeast, on MSSA and MRSA strains. Based on the findings of this study, the compounds produced by this yeast can be used to control S. aureus infections; however, further similar studies should be conducted to confirm the findings of the present study.
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24. Hoseini S, Niakan M, Saderi H, Emaneini M. Comparison of cefoxitin disk diffusion and PCR for mecA gene methods for detection of methicillin resistant Staphylococcus aureus. Daneshvar Med 2015;22: 41-46.
25. Srinivas B, Rani GS, Kumar BK, Chandrasekhar B, Krishna KV, Devi TA, et al. Evaluating the probiotic and therapeutic potentials of Saccharomyces cerevisiae strain (OBS2) isolated from fermented nectar of toddy palm. AMB Express 2017; 7: 2.
26. Lima MDSF, Souza KMS, Albuquerque WWC, Teixeira JAC, Cavalcanti MTH, Porto ALF. Saccharomyces cerevisiae from Brazilian kefir-fermented milk: An in vitro evaluation of probiotic properties. Microb Pathog 2017; 110: 670-677.
27. McCarthy H, Rudkin JK, Black NS, Gallagher L, O'Neill E, O'Gara JP. Methicillin resistance and the biofilm phenotype in Staphylococcus aureus. Front Cell Infect Microbiol 2015; 5: 1.
28. Walencka E, Wieckowska-Szakiel M, Rozalska S, Sadowska B, Rozalska B. A surface-active agent from Saccharomyces cerevisiae influences staphylococcal adhesion and biofilm development. Z Naturforsch C 2007; 62: 433-438.
29. Melo TA, Dos Santos TF, de Almeida ME, Junior LA, Andrade EF, Rezende RP, et al. Inhibition of Staphylococcus aureus biofilm by Lactobacillus isolated from fine cocoa. BMC Microbiol 2016; 16: 250.
30. Merghni A, Dallel I, Noumi E, Kadmi Y, Hentati H, Tobji S, et al. Antioxidant and antiproliferative potential of biosurfactants isolated from Lactobacillus casei and their anti-biofilm effect in oral Staphylococcus aureus strains. Microb Pathog 2017; 104: 84-89.
31. Even S, Charlier C, Nouaille S, Ben Zakour NL, Cretenet M, Cousin FJ, et al. Staphylococcus aureus virulence expression is impaired by Lactococcus lactis in mixed cultures. Appl Environ Microbiol 2009; 75: 4459-4472.
32. Parsaeimehr M, Azizkhani M, Jebelli Javan A. The inhibitory effects of 2 commercial probiotic strains on the growth of Staphylococcus aureus and gene expression of enterotoxin A. Int J Enteric Pathog 2017; 5: 70-75.
2. Charlier C, Cretenet M, Even S, Le Loir Y. Interactions between Staphylococcus aureus and lactic acid bacteria: an old story with new perspectives. Int J Food Microbiol 2009; 131: 30-39.
3. Berube BJ, Bubeck Wardenburg J. Staphylococcus aureus alpha-toxin: nearly a century of intrigue. Toxins (Basel) 2013; 5: 1140-1166.
4. Haugwitz U, Bobkiewicz W, Han SR, Beckmann E, Veerachato G, Shaid S, et al. Pore-forming Staphylococcus aureus alpha-toxin triggers epidermal growth factor receptor-dependent proliferation. Cell Microbiol 2006; 8: 1591-1600.
5. Argudin MA, Mendoza M, Rodicio MR. Food poisoning and Staphylococcus aureus enterotoxins. Toxins (Basel) 2010; 2: 1751-1773.
6. Hu DL, Nakane A. Mechanisms of staphylococcal enterotoxin-induced emesis. Eur J Pharmacol 2014; 722: 95-107.
7. Balaban N, Rasooly A. Staphylococcal enterotoxins. Int J Food Microbiol 2000; 61: 1-10.
8. Otto M (2008). Staphylococcal Biofilms. In: Bacterial biofilms. Ed, T. Romeo. Springer. Berlin Heidelberg.
9. Arciola CR, Campoccia D, Speziale P, Montanaro L, Costerton JW. Biofilm formation in Staphylococcus implant infections. A review of molecular mechanisms and implications for biofilm-resistant materials. Biomaterials 2012; 33: 5967-5982.
10. Rohinishree YS, Negi PS. Effect of licorice extract on cell viability, biofilm formation and exotoxin production by Staphylococcus aureus. J Food Sci Technol 2016; 53: 1092-1100.
11. Shokri D, Khorasgani MR, Mohkam M, Fatemi SM, Ghasemi Y, Taheri-Kafrani A. The Inhibition effect of Lactobacilli against growth and biofilm formation of Pseudomonas aeruginosa. Probiotics Antimicrob Proteins 2018; 10: 34-42.
12. Fakruddin M, Hossain MN, Ahmed MM. Antimicrobial and antioxidant activities of Saccharomyces cerevisiae IFST062013, a potential probiotic. BMC Complement Altern Med 2017; 17: 64.
13. Hatoum R, Labrie S, Fliss I. Antimicrobial and probiotic properties of yeasts: from fundamental to novel applications. Front Microbiol 2012; 3: 421.
14. Tahmasebi T, Nosrati R, Zare H, Saderi H, Moradi R, Owlia P. Isolation of indigenous Glutathione producing Saccharomyces cerevisiae strains. Iran J Pathol 2016;11: 354-362.
15. Moradi R, Nosrati R, Zare H, Tahmasebi T, Saderi H, Owlia P. Screening and characterization of in-vitro probiotic criteria of Saccharomyces and Kluyveromyces strains. Iran J Microbiol 2018;10: 123-131.
16. Krasowska A, Murzyn A, Dyjankiewicz A, Lukaszewicz M, Dziadkowiec D. The antagonistic effect of Saccharomyces boulardii on Candida albicans filamentation, adhesion and biofilm formation.FEMS Yeast Res 2009; 9: 1312-1321.
17. Liu D, Zeng X-A, Sun D-W, Han Z. Disruption and protein release by ultrasonication of yeast cells. Innov Food Sci Emerg Technol 2013; 18: 132-137.
18. CLSI. Methods for Dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard. M7-A9. 2012.
19. Zmantar T, Kouidhi B, Miladi H, Mahdouani K, Bakhrouf A. A microtiter plate assay for Staphylococcus aureus biofilm quantification at various pH levels and hydrogen peroxide supplementation. New Microbiol 2010; 33: 137-145.
20. Stepanovic S, Vukovic D, Hola V, Di Bonaventura G, Djukic S, Cirkovic I, et al. 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.
21. Fonseca AP, Extremina C, Fonseca AF, Sousa JC. Effect of subinhibitory concentration of piperacillin/tazobactam on Pseudomonas aeruginosa. J Med Microbiol 2004; 53: 903-910.
22. Shi C, Zhao X, Li W, Meng R, Liu Z, Liu M, et al. Inhibitory effect of totarol on exotoxin proteins hemolysin and enterotoxins secreted by Staphylococcus aureus. World J Microbiol Biotechnol 2015; 31: 1565-1573.
23. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408.
24. Hoseini S, Niakan M, Saderi H, Emaneini M. Comparison of cefoxitin disk diffusion and PCR for mecA gene methods for detection of methicillin resistant Staphylococcus aureus. Daneshvar Med 2015;22: 41-46.
25. Srinivas B, Rani GS, Kumar BK, Chandrasekhar B, Krishna KV, Devi TA, et al. Evaluating the probiotic and therapeutic potentials of Saccharomyces cerevisiae strain (OBS2) isolated from fermented nectar of toddy palm. AMB Express 2017; 7: 2.
26. Lima MDSF, Souza KMS, Albuquerque WWC, Teixeira JAC, Cavalcanti MTH, Porto ALF. Saccharomyces cerevisiae from Brazilian kefir-fermented milk: An in vitro evaluation of probiotic properties. Microb Pathog 2017; 110: 670-677.
27. McCarthy H, Rudkin JK, Black NS, Gallagher L, O'Neill E, O'Gara JP. Methicillin resistance and the biofilm phenotype in Staphylococcus aureus. Front Cell Infect Microbiol 2015; 5: 1.
28. Walencka E, Wieckowska-Szakiel M, Rozalska S, Sadowska B, Rozalska B. A surface-active agent from Saccharomyces cerevisiae influences staphylococcal adhesion and biofilm development. Z Naturforsch C 2007; 62: 433-438.
29. Melo TA, Dos Santos TF, de Almeida ME, Junior LA, Andrade EF, Rezende RP, et al. Inhibition of Staphylococcus aureus biofilm by Lactobacillus isolated from fine cocoa. BMC Microbiol 2016; 16: 250.
30. Merghni A, Dallel I, Noumi E, Kadmi Y, Hentati H, Tobji S, et al. Antioxidant and antiproliferative potential of biosurfactants isolated from Lactobacillus casei and their anti-biofilm effect in oral Staphylococcus aureus strains. Microb Pathog 2017; 104: 84-89.
31. Even S, Charlier C, Nouaille S, Ben Zakour NL, Cretenet M, Cousin FJ, et al. Staphylococcus aureus virulence expression is impaired by Lactococcus lactis in mixed cultures. Appl Environ Microbiol 2009; 75: 4459-4472.
32. Parsaeimehr M, Azizkhani M, Jebelli Javan A. The inhibitory effects of 2 commercial probiotic strains on the growth of Staphylococcus aureus and gene expression of enterotoxin A. Int J Enteric Pathog 2017; 5: 70-75.
| Files | ||
| Issue | Vol 11 No 3 (2019) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v11i3.1331 | |
| Keywords | ||
| Biofilm Exotoxins Probiotic Saccharomyces cerevisiae Staphylococcus aureus | ||
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How to Cite
1.
Saidi N, Owlia P, Amin Marashi SM, Saderi H. Inhibitory effect of probiotic yeast Saccharomyces cerevisiae on biofilm formation and expression of α-hemolysin and enterotoxin A genes of Staphylococcus aureus. Iran J Microbiol. 2019;11(3):246-254.
