Synergistic antibacterial effects of carvacrol and ε-polylysine
Main Article Content
Keywords
carvacrol, ε-polylysine, synergistic antimicrobial activity
Abstract
This study aimed to evaluate the antimicrobial efficacy of the combination of ɛ-polylysine (ɛ-PL) and carvacrol (Car) against foodborne pathogens, Escherichia coli and Staphylococcus aureus. The minimum inhibitory concentrations (MICs) of ɛ-PL (Car) against E. coli and S. aureus were 25 μg/mL (320 μg/mL) and 12.5 μg/mL (320 μg/mL), respectively. Checkerboard assays showed that the combination of ɛ-PL and Car exerted synergistic effects against E. coli and S. aureus with fraction inhibitory concentration index (FICI) of 0.375 and 0.5, respectively. It demonstrated that the combination of ɛ-PL and Car significantly inhibited the growth of the two strains compared to single treatment. Furthermore, the mode of action of ɛ-PL (6.25 μg/mL) or Car (80 μg/mL) in inhibiting E. coli and S. aureus was researched by assessing their changes with regard to cellular membrane integrity, membrane permeability, respiratory activity, and membrane structure. A combination of ɛ-PL and Car increased the damage to cell membranes and their permeability and led to the release of 260 nm absorbing materials, decreased respiratory-chain dehydrogenase activity compared with ɛ-PL or Car treatment alone. These results demonstrated that the combination of ɛ-PL and Car could be used as a new promising naturally sourced food preservative.
References
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Dorman, H. and Deans, S.G., 2010. Antimicrobial agents from plants: antibacterial activity of plant volatile oils. Journal of Applied Microbiology 88(2): 308–316. 10.1046/j.1365-2672.2000.00969.x
Filomena, N., Florinda, F., Laura, D.M., Raffaele, C. and Vincenco, D.F., 2013. Effect of essential oils on pathogenic bacteria. Food Control 6(12): 1451–1474. 10.3390/ph6121451
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Khlaifat, A.M., Al-limoun, M.O., Khleifat, K.M., Al Tarawneh, A.A., Qaralleh, H., Rayyan, E. and Alsharafa, K.Y., 2019. Antibacterial synergy of Tritirachium oryzae-produced silver nanoparticles with different antibiotics and essential oils derived from Cupressus sempervirens and Asteriscus graveolens (Forssk). Tropical Journal of Pharmaceutical research 18(12): 2605–2616. 10.4314/tjpr.v18i12.21
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Lambert, R.J.W., Skandamis, P.N., Coote P.J. and Nychas, G.J.E., 2001. A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. Journal of Applied Microbiology 91(3): 453–462. 10.1046/j.1365-2672.2001.01428.x
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Lin, L., Zhu, Y.L. and Cui, H.Y., 2018. Electrospun thyme essential oil/gelatin nanofibers for active packaging against Campylobacter jejuni in chicken. LWT-Food Science and Technology 97: 711–718. 10.1016/j.lwt.2018.08.015
Liu, H.X., Pei, H.B., Han, Z.N., Feng, G.L. and Li, D.P., 2015. The antimicrobial effects and synergistic antibacterial mechanism of the combination of epsilon-polylysine and nisin against Bacillus subtilis. Food Control 47: 444–450. 10.1016/j.foodcont.2014.07.050
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Miya, S., Takahashi, H., Hashimoto, M., Nakazawa, M., Kuda, T., Koiso, H. and Kimura, B., 2016. Development of a controlling method for Escherichia coli O157: H7 and Salmonella spp. in fresh market beef by using polylysine and modified atmosphere packaging. Food Control 37: 62–67. 10.1016/j.foodcont.2013.09.028
Oliveira, C.E.V., Stamford, T.L.M., Neto, N.J.G. and De Souza, E.L., 2010. Inhibition of Staphylococcus aureus in broth and meat broth using synergies of phenolics and organic acids. International Journal of Food Microbiology 137: 312–316. 10.1016/j.ijfoodmicro.2009.11.019
Palaniappan, K. and Holley, R.A., 2010. Use of natural antimicrobials to increase antibiotic susceptibility of drug resistant bacteria. International Journal of Food Microbiology 140(2–3): 164–168. 10.1016/j.ijfoodmicro.2010.04.001
Pei, R.S., Zhou, F., Ji, B.P. and Xu, J., 2009. Evaluation of combined antibacterial effects of eugenol, cinnamaldehyde, thymol, and carvacrol against E-coli with an improved method. Journal of Food Science 74(7): M379–M383. 10.1111/j.1750-3841.2009.01287.x
Pinilla, C.M.B. and Brandelli, A., 2016. Antimicrobial activity of nanoliposomes co-encapsulating nisin and garlic extract against Gram-positive and Gram-negative bacteria in milk. Innovative Food Science and Emerging Technologies 36: 287–293. 10.1016/j.ifset.2016.07.017
Saharkhiz, M.J., Zomorodian, K., Taban, A., Pakshir, K., Heshmati, K. and Rahimi, M.J., 2016. Chemical composition and antimicrobial activities of three satureja species against food-borne pathogens. Journal of Essential oil Bearing Plants 19(8): 1984–1992. 10.1080/0972060X.2016.1252697
Sharma, K., Guleria, S., Razdan, V.K. and Babu, V., 2020. Synergistic antioxidant and antimicrobial activities of essential oils of some selected medicinal plants in combination and with synthetic compounds. Industrial Crops and Products 154: 112569. 10.1016/j.indcrop.2020.112569
Shi, C., Zhao, X.C., Meng, R.Z., Liu, Z.J., Zhang, G.N. and Guo, N., 2017. Synergistic vantimicrobial effects of nisin and p-Anisaldehyde on Staphylococcus aureus in pasteurized milk. LWT-Food Science and Technology 84: 222–230. 10.1016/j.lwt.2017.05.056
Shima, S., Matsuoka, H., Iwamoto, T. and Sakai, H., 1984. Antimicrobial action of ε-poly-L-lysine. Journal of Antibiotics 37(11): 1449–1455. 10.7164/antibiotics.37.1449
Sondi, I. and Salopek-Sondi, B., 2004. Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. Journal of Colloid & Interface Science 275: 177–182. 10.1016/j.jcis.2004.02.012
Sun, G.Z., Yang, Q.C., Zhang, A.C., Guo, J., Liu, X.J., Wang, Y. and Ma, Q., 2018. Synergistic effect of the combined bio-fungicides ε-poly-l-lysine and chitooligosaccharide in controlling grey mould (Botrytis cinerea) in tomatoes. International Journal of Food Microbiology 276: 46–53. 10.1016/j.ijfoodmicro.2018.04.006
Sun, Z.L., Li, P.P., Liu, F., Bian, H., Wang, D.Y., Wang, X.M., Zou, Y., Sun, C. and Xu, W.M., 2017. Synergistic antibacterial mechanism of the Lactobacillus crispatus surface layer protein and nisin on Staphylococcus saprophyticus. Scientific Reports 7(1): 265. 10.1038/s41598-017-00303-8
Swamy, M.K., Akhtar, M.S. and Sinniah, U.R., 2016. Antimicrobial properties of plant essential oils against human pathogens and their mode of action: an updated review. Evidence-Based Complementary and Alternative Medicine 2016 (3012462): 3012462. 10.1155/2016/3012462
Teethaisong, Y., Autarkool, N., Sirichaiwetchakoon, K., Krubphachaya, P., Kupittayanant, S. and Eumkeb, G., 2014. Synergistic activity and mechanism of action of Stephania suberosa Forman extract and ampicillin combination against ampicillin-resistant Staphylococcus aureus. Journal of Biomedical Science 21(1): 90. 10.1186/s12929-014-0090-2
Ultee, A., Kets, E.P. and Smid, E.J., 1999. Mechanisms of action of carvacrol on the food-borne pathogen Bacillus cereus. Applied and Environmental Microbiology 65(10): 4606–4610. 10.1128/aem.65.10.4606-4610.1999
Vergis, J., Gokulakrishnan, P., Agarwal, R.K. and Kumar, A., 2015. Essential oils as natural food antimicrobial agents: a review. Critical Reviews in Food Science and Nutrition 55(10): 1320–1323. 10.1080/10408398.2012.692127
Wijesundara, N.M., Lee, S.F., Cheng, Z.Y., Davidson, R. and Rupasinghe, H.P.V., 2021. Carvacrol exhibits rapid bactericidal activity against Streptococcus pyogenes through cell membrane damage. Science Reports 11(1): 1487. 10.1038/s41598-020-79713-0
Windiasti, G., Feng, J.S., Ma, L.N., Hu, Y.X., Hakeem, M.J., Amoaka, K., Delaquis, P. and Lu, X.N., 2019. Investigating the synergistic antimicrobial effect of carvacrol and zinc oxide nanoparticles against Campylobacter jejuni. Food Control 96: 39–46. 10.1016/j.foodcont.2018.08.028
Wu, V.C.H., Qiu, X.J., de los Reyes, B.G., Lin, C.S. and Pan, Y.P., 2009. Application of cranberry concentrate (Vaccinium macrocarpon) to control Escherichia coli O157: H7 in ground beef and its antimicrobial mechanism related to the downregulated slp, hdeA and cfa. Food Microbiology 26(1): 32–38. 10.1016/j.fm.2008.07.014
Zahi, M.R., El Hattab, M., Liang, H. and Yuan, Q., 2017. Enhancing the antimicrobial activity of d-limonene nanoemulsion with the inclusion of ε-polylysine. Food Chemistry 221: 18–23. 10.1016/j.foodchem.2016.10.037
Zanini, S.F., Silva-Angulo, A.B., Rosenthal, A., Rodrigo, D. and Martinez, A., 2014. Effect of citral and carvacrol on the susceptibility of Listeria monocytogenes and Listeria innocua to antibiotics. Letters in Applied Microbiology 58(5): 486–492. 10.1111/lam.12218
Zhang, X.W., Shi, C., Liu, Z.J., Pan, F.G., Meng, R.Z. Bu, X.J., Xing, H.Q. Deng, Y.H., Guo, N. and Yu, L., 2018. Antibacterial activity and mode of action of ε-polylysine against Escherichia coli O157: H7. Journal of Medical Microbiology 67: 838–845. 10.1099/jmm.0.000729
Cao, Y.F., Zhou, D.G., Zhang, X.W., Xiao, X.L., Yu, Y.G. and Li, X.F., 2021. Synergistic effect of citral and carvacrol and their combination with mild heat against Cronobacter sakazakii CICC 21544 in reconstituted infant formula. LWT-Food Science and Technology 138: 110617. 10.1016/j.lwt.2020.110617
Chen, H.Q. and Zhong, Q.X., 2017. Lactobionic acid enhances the synergistic effect of nisin and thymol against Listeria monocytogenes Scott A in tryptic soy broth and milk. International Journal of Food Microbiology 260: 36–41. 10.1016/j.ijfoodmicro.2017.08.013
Cui, H.Y., Dai, Y.J. and Lin, L., 2018. Enhancing antibacterial efficacy of nisin in pork by poly-γ-glutamic acid/poly-l-lysine nanoparticles encapsulation. Journal of Food Safety 38(4): e12475. 10.1111/jfs.12475
De Souza, V.V.M.A., Crippa, B.L., De Almeida, J.M., Iacuzio, R., Setzer, W.N., Sharifi-Rad, J. and Cirone Silva, N.C., 2020. Synergistic antimicrobial action and effect of active chitosangelatin biopolymeric films containing Thymus vulgaris, Ocimum basilicum and Origanum majorana essential oils against Escherichia coli and Staphylococcus aureus. Cellular and Molecular Biology 66(4): 214–223. 10.14715/cmb/2020.66.4.26
Dorman, H. and Deans, S.G., 2010. Antimicrobial agents from plants: antibacterial activity of plant volatile oils. Journal of Applied Microbiology 88(2): 308–316. 10.1046/j.1365-2672.2000.00969.x
Filomena, N., Florinda, F., Laura, D.M., Raffaele, C. and Vincenco, D.F., 2013. Effect of essential oils on pathogenic bacteria. Food Control 6(12): 1451–1474. 10.3390/ph6121451
Govaris, A., Solomakos, N., Pexara, A. and Chatzopoulou, P.S., 2010. The antimicrobial effect of oregano essential oil, nisin and their combination against Salmonella Enteritidis in minced sheep meat during refrigerated storage. International Journal of Food Microbiology 137(2): 175–180. 10.1016/j.ijfoodmicro.2009.12.017
Guarda, A., Rubilar, J.F., Miltz, J. and Galotto, M.J., 2011. The antimicrobial activity of microencapsulated thymol and carvacrol, International Journal of Food Microbiology 146(2): 144–150. 10.1016/j.ijfoodmicro.2011.02.011
Khlaifat, A.M., Al-limoun, M.O., Khleifat, K.M., Al Tarawneh, A.A., Qaralleh, H., Rayyan, E. and Alsharafa, K.Y., 2019. Antibacterial synergy of Tritirachium oryzae-produced silver nanoparticles with different antibiotics and essential oils derived from Cupressus sempervirens and Asteriscus graveolens (Forssk). Tropical Journal of Pharmaceutical research 18(12): 2605–2616. 10.4314/tjpr.v18i12.21
Kozak, S.M., Brown, S.R.B., Bobak, Y. and D’Amico, D.J., 2018. Control of Listeria monocytogenes in whole milk using antimicrobials applied individually and in combination. Journal of Dairy Science 101(3): 1889–1900. 10.3168/jds.2017-13648
Lambert, R.J.W., Skandamis, P.N., Coote P.J. and Nychas, G.J.E., 2001. A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. Journal of Applied Microbiology 91(3): 453–462. 10.1046/j.1365-2672.2001.01428.x
Li, Y.Q., Han, Q., Feng, J.L., Tian, W.L. and Mo, H.Z., 2014. Antibacterial characteristics and mechanisms of ɛ-poly-lysine against Escherichia coli and Staphylococcus aureus. Food Control 43: 22–27. 10.1016/j.foodcont.2014.02.023
Lin, L., Zhu, Y.L. and Cui, H.Y., 2018. Electrospun thyme essential oil/gelatin nanofibers for active packaging against Campylobacter jejuni in chicken. LWT-Food Science and Technology 97: 711–718. 10.1016/j.lwt.2018.08.015
Liu, H.X., Pei, H.B., Han, Z.N., Feng, G.L. and Li, D.P., 2015. The antimicrobial effects and synergistic antibacterial mechanism of the combination of epsilon-polylysine and nisin against Bacillus subtilis. Food Control 47: 444–450. 10.1016/j.foodcont.2014.07.050
Lv, F., Liang, H., Yuan, Q.P. and Li, C.F., 2011. In vitro antimicrobial effects and mechanism of action of selected plant essential oil combinations against four food-related microorganisms. Food Research International 44(9): 3057–3064. 10.1016/j.foodres.2011.07.030
Miya, S., Takahashi, H., Hashimoto, M., Nakazawa, M., Kuda, T., Koiso, H. and Kimura, B., 2016. Development of a controlling method for Escherichia coli O157: H7 and Salmonella spp. in fresh market beef by using polylysine and modified atmosphere packaging. Food Control 37: 62–67. 10.1016/j.foodcont.2013.09.028
Oliveira, C.E.V., Stamford, T.L.M., Neto, N.J.G. and De Souza, E.L., 2010. Inhibition of Staphylococcus aureus in broth and meat broth using synergies of phenolics and organic acids. International Journal of Food Microbiology 137: 312–316. 10.1016/j.ijfoodmicro.2009.11.019
Palaniappan, K. and Holley, R.A., 2010. Use of natural antimicrobials to increase antibiotic susceptibility of drug resistant bacteria. International Journal of Food Microbiology 140(2–3): 164–168. 10.1016/j.ijfoodmicro.2010.04.001
Pei, R.S., Zhou, F., Ji, B.P. and Xu, J., 2009. Evaluation of combined antibacterial effects of eugenol, cinnamaldehyde, thymol, and carvacrol against E-coli with an improved method. Journal of Food Science 74(7): M379–M383. 10.1111/j.1750-3841.2009.01287.x
Pinilla, C.M.B. and Brandelli, A., 2016. Antimicrobial activity of nanoliposomes co-encapsulating nisin and garlic extract against Gram-positive and Gram-negative bacteria in milk. Innovative Food Science and Emerging Technologies 36: 287–293. 10.1016/j.ifset.2016.07.017
Saharkhiz, M.J., Zomorodian, K., Taban, A., Pakshir, K., Heshmati, K. and Rahimi, M.J., 2016. Chemical composition and antimicrobial activities of three satureja species against food-borne pathogens. Journal of Essential oil Bearing Plants 19(8): 1984–1992. 10.1080/0972060X.2016.1252697
Sharma, K., Guleria, S., Razdan, V.K. and Babu, V., 2020. Synergistic antioxidant and antimicrobial activities of essential oils of some selected medicinal plants in combination and with synthetic compounds. Industrial Crops and Products 154: 112569. 10.1016/j.indcrop.2020.112569
Shi, C., Zhao, X.C., Meng, R.Z., Liu, Z.J., Zhang, G.N. and Guo, N., 2017. Synergistic vantimicrobial effects of nisin and p-Anisaldehyde on Staphylococcus aureus in pasteurized milk. LWT-Food Science and Technology 84: 222–230. 10.1016/j.lwt.2017.05.056
Shima, S., Matsuoka, H., Iwamoto, T. and Sakai, H., 1984. Antimicrobial action of ε-poly-L-lysine. Journal of Antibiotics 37(11): 1449–1455. 10.7164/antibiotics.37.1449
Sondi, I. and Salopek-Sondi, B., 2004. Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. Journal of Colloid & Interface Science 275: 177–182. 10.1016/j.jcis.2004.02.012
Sun, G.Z., Yang, Q.C., Zhang, A.C., Guo, J., Liu, X.J., Wang, Y. and Ma, Q., 2018. Synergistic effect of the combined bio-fungicides ε-poly-l-lysine and chitooligosaccharide in controlling grey mould (Botrytis cinerea) in tomatoes. International Journal of Food Microbiology 276: 46–53. 10.1016/j.ijfoodmicro.2018.04.006
Sun, Z.L., Li, P.P., Liu, F., Bian, H., Wang, D.Y., Wang, X.M., Zou, Y., Sun, C. and Xu, W.M., 2017. Synergistic antibacterial mechanism of the Lactobacillus crispatus surface layer protein and nisin on Staphylococcus saprophyticus. Scientific Reports 7(1): 265. 10.1038/s41598-017-00303-8
Swamy, M.K., Akhtar, M.S. and Sinniah, U.R., 2016. Antimicrobial properties of plant essential oils against human pathogens and their mode of action: an updated review. Evidence-Based Complementary and Alternative Medicine 2016 (3012462): 3012462. 10.1155/2016/3012462
Teethaisong, Y., Autarkool, N., Sirichaiwetchakoon, K., Krubphachaya, P., Kupittayanant, S. and Eumkeb, G., 2014. Synergistic activity and mechanism of action of Stephania suberosa Forman extract and ampicillin combination against ampicillin-resistant Staphylococcus aureus. Journal of Biomedical Science 21(1): 90. 10.1186/s12929-014-0090-2
Ultee, A., Kets, E.P. and Smid, E.J., 1999. Mechanisms of action of carvacrol on the food-borne pathogen Bacillus cereus. Applied and Environmental Microbiology 65(10): 4606–4610. 10.1128/aem.65.10.4606-4610.1999
Vergis, J., Gokulakrishnan, P., Agarwal, R.K. and Kumar, A., 2015. Essential oils as natural food antimicrobial agents: a review. Critical Reviews in Food Science and Nutrition 55(10): 1320–1323. 10.1080/10408398.2012.692127
Wijesundara, N.M., Lee, S.F., Cheng, Z.Y., Davidson, R. and Rupasinghe, H.P.V., 2021. Carvacrol exhibits rapid bactericidal activity against Streptococcus pyogenes through cell membrane damage. Science Reports 11(1): 1487. 10.1038/s41598-020-79713-0
Windiasti, G., Feng, J.S., Ma, L.N., Hu, Y.X., Hakeem, M.J., Amoaka, K., Delaquis, P. and Lu, X.N., 2019. Investigating the synergistic antimicrobial effect of carvacrol and zinc oxide nanoparticles against Campylobacter jejuni. Food Control 96: 39–46. 10.1016/j.foodcont.2018.08.028
Wu, V.C.H., Qiu, X.J., de los Reyes, B.G., Lin, C.S. and Pan, Y.P., 2009. Application of cranberry concentrate (Vaccinium macrocarpon) to control Escherichia coli O157: H7 in ground beef and its antimicrobial mechanism related to the downregulated slp, hdeA and cfa. Food Microbiology 26(1): 32–38. 10.1016/j.fm.2008.07.014
Zahi, M.R., El Hattab, M., Liang, H. and Yuan, Q., 2017. Enhancing the antimicrobial activity of d-limonene nanoemulsion with the inclusion of ε-polylysine. Food Chemistry 221: 18–23. 10.1016/j.foodchem.2016.10.037
Zanini, S.F., Silva-Angulo, A.B., Rosenthal, A., Rodrigo, D. and Martinez, A., 2014. Effect of citral and carvacrol on the susceptibility of Listeria monocytogenes and Listeria innocua to antibiotics. Letters in Applied Microbiology 58(5): 486–492. 10.1111/lam.12218
Zhang, X.W., Shi, C., Liu, Z.J., Pan, F.G., Meng, R.Z. Bu, X.J., Xing, H.Q. Deng, Y.H., Guo, N. and Yu, L., 2018. Antibacterial activity and mode of action of ε-polylysine against Escherichia coli O157: H7. Journal of Medical Microbiology 67: 838–845. 10.1099/jmm.0.000729
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