In collaboration with Scientific Association of Iranian Medicinal Plants

Document Type : Research Paper

Authors

1 Faculty of Veterinary Medicine, Amol University of Special Modern Technologies, Amol, Iran

2 Department of Microbiology and Ecology, University of Valencia

3 the Department of Biotechnology, Institute of Agro Chemical and Food Technology, Valencia, Spain

4 Department of Microbiology and Ecology, University of Valencia, Valencia, Spain

Abstract

Staphylococcal food poisoning is resulted from the consumption of a food in which enterotoxigenic staphylococci have grown and produced toxins. Targeting bacterial virulence factors is now gaining interest as an alternative strategy to develop new types of antimicrobial preservatives. The purpose of this study was to determine the effect of R. officianalis L. (Ros) essential oil (EO) on growth and gene expression of enterotoxins A, C, and E in Staphylococcus aureus ATCC 29213. In this study, after determining the minimum inhibitory concentration, the growth and secretion of SEA, SEC, and SEE (detected by ELISA method) by S. aureus treated with graded subinhibitory concentrations of EO was evaluated. In addition, the influence of the EO on the transcription of sea, sec and see (the genes encoding SEA, SEC and SEE, respectively) was analyzed by quantitative RT-PCR. Ros EO at a concentration of 75% MIC, significantly, reduced the growth of S. aureus. EO inhibited the transcription of sea, sec and see in S. aureus, in a dose-dependent manner, resulting in a reduction of SEA, SEC and SEE secretion. These data suggest that the Ros EO may be useful as a natural preservative against the growth and enterotoxin production of S.aureus in food industry.

Keywords

Adams, R.P., 2001. Identification of Essential Oils Components by Gas Chromatography/Quadrupole Mass Spectroscopy. Allured Publishing Corporation, Illinois, 469p.
- Anonymous, A., 2007. The community summary report on trends and sources of zoonoses, zoonotic agents, antimicrobial resistance and foodborne outbreaks in the European Union in 2006. European Food Safety Authority Journal, 130: 1-310.
- Asanova, Zh.K., Suleimenov, E.M., Atazhanova, G.A., Dembitskii, A.D., Pak, R.N., Dar, A. and Adekenov, S.M., 2003. Biological activity of 1,8-cineole from levant wormwood. Pharmaceutical Chemistry Journal, 37(1): 28-30.
- Balaban, N. and Rasooly, A., 2000. Staphylococcal enterotoxins. International Journal of Food Microbiology, 61: 1-10.
- Bernardo, K., Pakulat, N., Fleer, S., Schnaith, A., Utermöhlen, O., Krut O., Müller, S. and Krönke, M., 2004. Subinhibitory concentrations of linezolid reduce Staphylococcus aureus virulence factor expression. Antimicrobial Agents and Chemotherapy, 48(2): 546-555.
- Betley, M.J. and Mekalanos, J.J., 1988. Nucleotide sequence of the type A staphylococcal enterotoxin gene. Journal of Bacteriology, 170: 34-41.
- Bohach, G.A. and Schlievert, P.M., 1989. Conservation I biologically active portions of staphylococcal enterotoxins C1 and C2. Infections and Immunology, 57(7): 2249-2252.
- Borst, D.W. and Betley, M.J., 1994. Promoter analysis of the staphylococcal enterotoxin A gene. Journal of Biological Chemistry, 269(3): 1883-1888.
- Cegelski, L., Marshall, G.R., Eldridge, G.R. and Hultgren, S.J., 2008. The biology and future prospects of antivirulence therapies. Nature Reviews Microbiology, 6: 17-27.
- Couch, J.L., Soltis, M.T. and Betley, M.J., 1988. Cloning and nucleotide sequence of the type E staphylococcal enterotoxin gene. Journal of Bacteriology, 170: 2954-2960.
- Debersac, P., Haydel, J.M, Amiot, M.J, Goudonnet, H., Artue, Y., Suschetet, M. and Siess, M.H., 2001. Introduction of cytochrome P450 and/or dhietoxication enzymes by various extracts of rosemary description of specific patterns. Food and Chemical Technology, 39(9): 907-918.
- Escaich, S., 2008. Antivirulence as a new antibacterial approach for chemotherapy. Current Opinion in Cheical Biology, 12(4): 400-408.
- Fischer, A., Francios, P., Holtfreter, S., Broeker, B.M. and Schrenzel, J., 2009. Development and evaluation of a rapid strategy to determine enterotoxin gene content in Staphylococcus aureus. Journal of Microbiological Methods, 77(2): 184-190.
- Fu, Y.J., Zu, Y.G., Chen, L.Y., Shil, X.G., Wang, Z., Sunl, S. and Efferth, T., 2007a. Antimicrobial activity of clove and rosemary essential oils alone and in combination. PhytotherapyResearch, 21(10): 989-994.
- Fu, Y.J., Zu, Y.G., Chen, L.Y., Efferth, T., Lianch, H., Liu, Z. and Liu, W., 2007b. Investigation of antibacterial activity of rosemary essential oil against Propionibacterium acnes with atomic force microscopy. Planta Medica, 73(12): 1275-1280.
- Goerke, C., Fluckiger, U., Steinhuber, A., Zimmerli, W. and Wolz, C., 2001. Impact of the regulatory loci agr, sarA and sae of Staphylococcus aureus on the induction of alpha-toxin during device-related infection resolved by direct quantitative transcript analysis. Molecular Microbiology, 40(6): 1439-1447.
- Hennekinne, J.A., Brun, B., De Buyser, M.L., Dupuis, A., Ostyn, A. and Dragacci, S., 2009. Innovative application of mass spectrometry for the characterization of staphylococcal enterotoxins involved in food poisoning outbreaks. Apllied Environmental Microbiology, 75(3): 882-884.
- Herbert, S., Barry, P. and Novick, R.P., 2001. Subinhibitory clindamycin differentially inhibits transcription of exoprotein genes in Staphylococcus aureus. Infections and Immunology, 69(5): 2996-3003.
- Hu, D.L., Omoe, K., Inoue, F., Kasai, T., Yasujima, M., Shinagawa, K. and Nakane, K., 2008. Comparative prevalence of superantigenic toxin genes in meticillin-resistant and meticillin-susceptible Staphylococcus aureus isolates. Journal of Medical Microbiology, 57(9): 1106-1112.
- Huang, I.Y., Hughes, J.L., Bergdoll, M.S. and Schantz, E.J., 1987. Complete amino acid sequence of staphylococcal enterotoxin A. Journal of Biological Chemistry, 262(15): 7006-7013.
- Jamshidi, R., Afzali, Z. and Afzali, D., 2009. Chemical composition of hydrodistillation essential oil of rosemary in different origins in Iran and comparison with other countries. American-Eurasian Journal of Agricultural and EnvironmentalScience, 5(1): 78-81.
- Koszczol, C., Bernardo, K., Kronke, M. and Krut, O., 2006. Subinhibitory quinupristin/dalfopristin attenuates virulence of Staphylococcus aureus. Journal of Antimicrobial Chemotherapy, 58(3): 564-574.
- Kuroda, H., Kuroda, M., Cui, L. and Hiramatsu, K., 2007. Subinhibitory concentrations of beta-lactam induce haemolytic activity in Staphylococcus aureus through the SaeRS two-component system. FEMS Microbiology Letters, 268: 98-105.
- Moghtader, M. and Afzali, D., 2009. Study of the antibacterial properties of the essential oil of rosemary.American-Eurasian Journal of Agricultural and EnvironmentalScience, 5(3): 393-397.
- NCCLS (National Committee for Clinical Laboratory Standards)., 2000. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically. Approved Standard, M7-A5.
- Obeng-Ofori, D. and Reichmuth, C., 1997. Biological activity of eugenol, a major component of Ocimum suave (Wild.) against four species of stored product coleopteran. International Journal of Pest Management, 43: 89-94.
- Oussalah, M., Caillet, S., Saucier, L. and Lacroix, M., 2007. Inhibitory of selected plant essential oils on the growth of four pathogenic bacteria: E.coli O157:H7, salmonella typhimurium, Staphylococcus aureus and Listeria monocytogenes. Food Control, 18(5): 414-420.
- Parsaeimehr, M., Akhondzadeh Basti, A.A., Radmehr, B., Misaghi, A., Abbasifar, A., Karim, G., Rokni, N., Sobhani Motlagh, M., Gandomi, H., Noori, N. and Khanjari, A., 2010. Effect of Zataria multiflora Boiss. essential oil, nisin, and their combination on the production of enterotoxin C and alpha-hemolysin by Staphylococcus aureus. Foodborne Pathogens and Disease, 7(3): 456-463.
- Qiu, J., Wang, D., Xiang, H., Feng, H., Xia, L., Jiang, Y., Xia, L., Dong, J., Lu, J., Lu, Y. and Deng, X., 2010. Subinhibitory concentrations of thymol reduce enterotoxins A and B and a-hemolysin production in Staphylococcus aureus isolates. Plos ONE, 5(3): e9736.
- Recsei, P., Kreiswirth, B., O’Reilly, M., Schlievert, P., Gruss, A. and Novick, R.P., 1986. Regulation of exoprotein gene expression in Staphylococcus aureus by agr. Molecular and General Genetics, 202: 58-61.
- Rosec, J.P. and Gigaud, O., 2002. Staphylococcal enterotoxin genes of classical and new types detected by PCR in France. International Journal of Food Microbiology, 77(1-2): 61-70.
- Saei-Dehkordi, S.S., Tajik, H., Moradi, M. and Khalighi-Sigaroodi, F., 2010. Chemical composition of essential oils in Zataria multiflora Boiss. From different parts of Iran and their radical scavenging and antimicrobial activity. Food and Chemical Toxicology, 48(6): 1562-1567.
- Shah, S., Stapleton, P.D. and Taylor, P.W., 2008. The polyphenol (2)-epicatechin gallate disrupts the secretion of virulence-related proteins by Staphylococcus aureus. Letters in Applied Microbiology, 46(2): 181-185.
- Smith-Palmer, A., Steward, J. and Fyfe, L., 2001. The potential application of plant essential oils as natural preservatives in soft cheese. Food Microbiology, 18(4): 463-470.
- Smith-Palmer, A., Stewart, J. and Fyfe, L., 2004. Influence of subinhibitory concentrations of plant essential oils on the production of enterotoxins A and B and alpha-toxin by Staphylococcus aureus. Journal of Medical Microbiology, 53(10): 1023-1027.
- Stevens, D.L. Ma, Y., Salmi, D.B., Mclndoo, E., Wallace, R.J. and Bryant, A.E., 2007. Impact of antibiotics on expression of virulence-associated exotoxin genes in methicillinsensitive and methicillin-resistant Staphylococcus aureus. Journal of Infectious Diseases, 195(2): 202-211.
- Su, Y.C. and Wong, A.C.L., 1997. Current perspectives on detection of Staphylococcal enterotoxins. Journal of Food Protection, 60: 195-202.
- Tassou, C, Koutsoumanis, K. and Nychas, G.J.E., 2000. Inhibition of Salmonella enteritidis and Staphylococcus aureus in nutrient broth by mint essential oil. Food Research International, 33: 273-280.
- Tranter, H.S., Tassou, C.C. and Nychas, G.J.E., 1993.The effect of the olive phenolic compound, oleuropein, on growth and enterotoxin B production by Staphylococcus aureus. Journal of Applied Bacteriology, 74(3): 253-259.
- Tremaine, M.T., Brockman, D.K. and Betley, M.J., 1993. Staphylococcal enterotoxin A gene (sea) expression is not affected by the accessory gene regulator (agr). Infection and Immunology, 61: 356-359.
- Vasconcelos, N.G. and de Souza da Cunha, M.L.R., 2010. Staphylococcal enterotoxins: Molecular aspects and detection methods. Journal of Public Health Epidemiology, 2(3): 29-42.
- Vianello, M.A., 2006. Caracterização genotípica dos fatores de virulência e seu regulador agr em cepas de Staphylococcus aureus sensíveis à oxacilina. Faculdade de Ciências Farmacêuticas, São Paulo, 99p.