The Combined effect of Rosmarinus officinalis L essential oil and Bacteriocin BacLP01 from Lactobacillus plantarum against Bacillus subtilis ATCC11778 http://www.doi.org/10.26538/tjnpr/v7i3.14
Main Article Content
Abstract
Combining bacterial metabolites and natural products of plants is one proposed alternative to antibiotic usage. Reports on such combinations are starting to emerge. This study aimed to determine the antibacterial potential of bacteriocin (BacLP01) produced by Lactobacillus plantarum and the essential oil of Rosmarinus officinalis L (ROEO) alone and their combination. Each antibacterial agent was tested against food-borne pathogens: Bacillus subtilis, Bacillus cereus, Escherichia coli, and Staphylococcus aureus using the agar well diffusion method. The antibacterial agents were evaluated from their minimum inhibitory concentration (MIC) against the test organisms. The checkerboard technique was performed to assess the resulting combination to determine the nature of the sum effects between antibacterial agents against B. subtilis ATCC11778. BacLP01 achieved the highest activity against B. subtilis, equivalent to 6400 AU/mL. ROEO showed an inhibition zone ranging from 10.23 ± 1.92 to 14.52 ± 0.83mm. S. aureus expressed the highest sensitivity to ROEO (14.52 ± 0.83 mm), and B. subilis presented
low susceptibility with a 10.23± 1.92 mm diameter inhibition zone. Likewise, the synergistic effect of their combination on B. subilis ATCC11778 follows the same trend. The MICs for bacteriocin (BacLP01) and ROEO were 5 and 6.25 μL/mL, respectively. The result from FICI for the combination of BacLP01 and ROEO was 0.49, suggesting a synergistic interaction effect
against B. subtilis. The study concluded that a combination of BacLP01 and ROEO could be an
efficient means to control the presence of pathogenic bacteria in food.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
References
Martin RA, Maurice M. Food Microbiology. Cambridge: Royal Society of Chemistry, 2007.
Gopal N, Hill C, Ross PR, Beresford TP, Fenelon MA, Cotter PD. The Prevalence and Control of Bacillus and Related Spore-Forming Bacteria in the Dairy Industry. Front Microbiol. 2015;6:1–18.
He S, Hu Y, Zhang S, Wang D, Wu Y, Gao Y. Evaluation of Bacillus subtilis spore contamination in dairy products in China. Food Control. 2019;(105):122–127.
Zhang H, Zhao L, Li X, Li Y, Cui F, Sun Y. Enhanced production of surfactin from Bacillus subtilis by a stepwise pH control strategy. Bioprocess Biosyst Eng. 2018;41(1):93-101.
Brantl S, Müller P. Toxin–Antitoxin Systems in Bacillus subtilis. Toxins (Basel) .2019;11(5):262.
Mun SY, Kim SK, Woo ER, Chang HC. Purification and characterisation of an antimicrobial compound produced by Lactobacillus plantarum EM showing both antifungal and antibacterial activities. LWT. 2019;114(4):108403.
Oussalah M, Caillet S, Saucier L, Lacroix M. Inhibitory effects 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, 2007;18(5):414–420.
Bungenstock L, Abdulmawjood A, Reich F. Evaluation of antibacterial properties of lactic acid bacteria from traditionally and industrially produced fermented sausages from Germany. PLoS. 2020;15(3):e0230345.
9Chikindas ML, Weeks R, Drider D, Chistyakov VA, Dicks LM. Functions and emerging applications of bacteriocins. Curr Opin Biotechnol. 2018;49:23–28.
González-Rodrı́guez M-N, Sanz J-J, Santos J-Á, Otero A, Garcıá -López M-L. Numbers and types of microorganisms in vacuum-packed cold-smoked freshwater fish at the retail level. Int J Food Microbiol. 2002;77(1–2):161–168.
Rota C, Carramiñana Jj, Burillo J, Herrera A. In Vitro Antimicrobial Activity of Essential Oils from Aromatic Plants against Selected Food-borne Pathogens. J Food Prot. 2004;67(6):1252–1256.
Burt SA, Reinders RD. Antibacterial activity of selected plant essential oils against Escherichia coli O157:H7. Lett Appl Microbiol. 2003;36(3):162–167.
Burt S. Essential oils: their antibacterial properties and potential applications in foods—a review. Int J Food Microbiol. 2004;94(3):223–253.
Tongnuanchan P, Benjakul S. Essential Oils: Extraction, Bioactivities, and Their Uses for Food Preservation. J
Food Sci. 2014;79(7):R1231–R1249.
Bakkali F, Averbeck S, Averbeck D, Idaomar M. Biological effects of essential oils – A review. Food Chem Toxicol. 2008;46(2):446–475.
SHELEF LA. Antimicrobial Effects of Spices. J Food Saf. 1984;6(1):29–44.
Nieto G, Ros G, Castillo J. Antioxidant and Antimicrobial Properties of Rosemary (Rosmarinus officinalis L): A Review. Medicines. 2018;5(3):98.
Karsha P V., Lakshmi T. Antimicrobial activity of essential oils against foodborne pathogens and spoilage bacteria in model food systems: A review. Crit Rev Food Sci Nutr. 2020;60(21):3569–3585.
Khameneh B, Iranshahy M, Soheili V. Review on plant antimicrobials: a mechanistic viewpoint. Antimicrob
Resist Infect Control. 2019;8(1):118.
Tala MF, Leal SM, Lima AS, Viana JMP, Maia JGS, Figueiredo LS. Chemical composition, antioxidant and antimicrobial activities of the essential oil of Rosmarinus officinalis L. from Maranhão, Brazil. J Essent Oil. 2019;31(3):31(3), 191-199.
Almariri MA, Al-Hammami AM, Alnimer MA. Chemical composition and antimicrobial activity of essential oils
from Thymus vulgaris, Rosmarinus officinalis, and Origanum majorana grown in Northern Jordan. J Essent Oil Bear Plants. 2019;22(2):478-488.
Baranauskienė R, Venskutonis PR, Dambrauskienė E. Essential oil composition and antimicrobial activity of Rosmarinus officinalis L. and Melissa officinalis L. collected in Lithuania. Ind Crops Prod. 2018;124:198– 204.
Ouadi Y El, Bahhar N, Bakri Y, Douch J, Chaouch A, Bali B El. Chemical composition and in vitro antioxidant and antibacterial activities of essential oils of Rosmarinus officinalis L. from Morocco. Int J Curr Microbiol Appl Sci. 2020;9(5):2385–2394.
Benamara R. N. Gemelas L., Ibri K. M-BB. and D. Sensory, microbiological and physico-chemical characterisation of Klila, a traditional cheese made in the south-west of Algeria. African J Microbiol Res. 2016;10(41):1728–1738.
Fleming HP, Etchells JL, Costilow RN. Microbial inhibition by an isolate of pediococcus from cucumber brines. Appl Microbiol. 1975;30(6):1040–2.
Castro MP, Rojas AM, Campos CA, Gerschenson LN. Effect of preservatives, tween 20, oil content and emulsion structure on the survival of Lactobacillus fructivorans in model salad dressings. LWT - Food Sci Technol. 2009;42(8):1428–1434.
Maqsood S, Hasan F, Masud T, Imran M. Preliminary characterisation of bacteriocin produced by Lactobacillus acidophilus TS1 isolated from traditional dahi. Ann Microbiol. 2008;58(4):617–622.
Saranraj, P., Sivasankar P. Characterization and application of bacteriocin produced by Lactobacillus acidophilus isolated from human gut. Microb Pathog. 2019;137:103774.
Yanagida F, Chen Y, Shinohara T. Searching for bacteriocin-producing lactic acid bacteria in soil. J Gen Appl Microbiol. 2006;52(1):21–28.
Vignolo GM, Kairuz MN de, Ruiz Holgado AAP de, Oliver G. Influence of growth conditions on the production of lactocin 705, a bacteriocin produced by Lactobacillus casei CRL 705. J Appl Bacteriol. 1995;78(1):5–10.
Marston A, Hostettmann K. Developments in the application of counter-current chromatography to plant analysis. J Chromatogr A. 2006;1112(1–2):181–194.
Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. 2020.
Ponce AG, Fritz R, Valle C del, Roura SI. Antimicrobial activity of essential oils on the native microflora of
organic Swiss chard. LWT - Food Sci Technol. 2003;36(7):679–684.
(EUCAST). EC on AST. Breakpoint tables for interpretation of MICs and zone diameters. Version 10.0. 2020.
Sanz-Puig M, Ramos-Vega A, Beltrán A, Roncalés P. Combination of bacteriocin and organic acid as a hurdle
technology to improve the shelf-life of beef patties. Foods. 2021;10(2):277.
Lacroix M. The Use of Essential Oils and Bacteriocins as Natural Antimicrobial and Antioxidant Compounds. Food. 2007;2:181–192.
Wang H, Zhou L, Dong X, Qu H, Feng X, Liu H. Antibacterial mechanism of oregano essential oil and its primary component carvacrol against Salmonella enteritidis. Food Control. 2020;108:106836.
Höltzel A, Gänzle MG, Nicholson GJ, Hammes WP, Jung G. The First Low Molecular Weight Antibiotic from Lactic Acid Bacteria: Reutericyclin, a New Tetramic Acid. Angew Chemie Int Ed. 2000;39(15):2766–2768.
Zommiti M, Feuilloley MGJ, Connil N. Biodiversity of bacteriocins and their activity against the Gram-negative bacteria Escherichia coli. J Appl Microbiol. 2017;123(3):706-719.
Javed A, Masud T, ul Ain Q, Imran M, Maqsood S. Enterocins of Enterococcus faecium, emerging natural food preservatives. Ann Microbiol. 2011;61(4):699–708.
Juarez-Tomas MS, Cascales-Pinol S, Rodriguez JM. Biotechnological applications of bacteriocins: recent trends and open prospects. Crit Rev Food Sci Nutr. 2019;59(5):817–835.
Garde S, Pandey A. Lactic acid bacteria: Biodiversity and taxonomy. In: Springer C, editor. Lactic acid bacteria. 2016; p. 1–20.
Ríos-Colombo NS, Rodríguez-Hernández AI, RiveraChavira BE, Olvera-Ramírez R. Characterization of bacteriocin-like substances produced by Lactobacillus plantarum strains isolated from traditional Mexican fermented foods. LWT. 2020;128:109447.
Feliatra F, Muchlisin ZA, Teruna HY, Utamy WR, Nursyirwani N, Dahliaty A. Potential of bacteriocins produced by probiotic bacteria isolated from tiger shrimp and prawns as antibacterial to Vibrio, Pseudomonas, and Aeromonas species on fish. F1000Research . 2018;7(1):415.
Wu Q, Zhang J, Hu X, et al. Characterisation of a novel bacteriocin produced by Lactobacillus plantarum Q180 isolated from fermented cucumbers. Food Control. 2019;98:1-8.
Jiang Y, Wu N, Fu Y, Wang W, Luo M. Chemical composition and antimicrobial activity of the essential oil of Rosemary. Environ Toxicol Pharmacol. 2011;32(1):63–68.
Bozin B, Mimica-Dukic N, Samojlik I, Jovin E. Antimicrobial and Antioxidant Properties of Rosemary and Sage (Rosmarinus officinalis L. and Salvia officinalis L., Lamiaceae) Essential Oils. J Agric Food Chem. 2007;55(19):7879–7885.
Santoyo S, Cavero S, Jaime L, Ibañez E, Señoráns FJ, Reglero G. Chemical composition and antimicrobial activity of Rosmarinus officinalis L. essential oil obtained via supercritical fluid extraction. J Food Prot. 2005;68(4):790–5.
Hendel N, Napoli E, Sarri M, et al. Essential Oil from Aerial Parts of Wild Algerian Rosemary: Screening of Chemical Composition, Antimicrobial and Antioxidant Activities. J Essent Oil Bear Plants. 2019;22(1):1–17.
Mehalaine S, Belfadel O, Menasria T, Messaili A. Chemical composition and antibacterial activity of essential oils of three medicinal plants from Algerian semi-arid climatic zone Composition chimique et activité antibactérienne des huiles essentielles de trois plantes médicinales récoltées de la région s. Phytothérapie. 2017.
Zaouali Y, Bouzaine T, Boussaid M. Essential oils composition in two Rosmarinus officinalis L. varieties and incidence for antimicrobial and antioxidant activities. Food Chem Toxicol. 2010;48(11):3144–3152.
Tural S, Durmaz Y, Urçar E, Turhan S. Antibacterial Activity of Thyme (Thymus vulgaris L.), Laurel (Lauris nobilis L.), Rosemary (Rosmarinus officinalis L.) and Parsley (Petroselinum crispum L.) Essential Oils against Some Fish Pathogenic Bacteria. Acta Aquat Turc. 2019;15(4):439–446.
López P, Sánchez C, Batlle R, Nerín C. Solid- and VaporPhase Antimicrobial Activities of Six Essential Oils: Susceptibility of Selected Foodborne Bacterial and Fungal Strains. J Agric Food Chem. 2005;53(17):6939– 6946.
Raeisi M, Tajik H, Aminzare M, et al. The Role of Nisin, Monolaurin, and EDTA in Antibacterial Effect of Rosmarinus Officinalis L and Cinnamomum Zeylanicum Blume Essential Oils on Foodborne Pathogens. J Essent Oil Bear Plants. 2016;19(7):1709–1720.
Bozin B, Mimica-Dukic N, Samojlik I, Jovin E. Antimicrobial and Antioxidant Properties of Rosemary and Sage (Rosmarinus officinalis L. and Salvia officinalis L., Lamiaceae) Essential Oils. J Agric Food Chem. 2007;55(19):7879–7885.
Pintore G, Usai M, Bradesi P, et al. Chemical composition and antimicrobial activity of Rosmarinus officinalis L. oils from Sardinia and Corsica. Flavour Fragr J. 2002;17(1):15–19.
Lin GS, Duan WG, Yang LX, Huang M, Lei FH. Synthesis and antifungal activity of novel myrtenal-based 4-Methyl-1,2,4-triazole-thioethers. Molecules 2017;22(2):4–13.
Roomiani L, Ghaeni M, Moarref M, Fallahi R, Lakzaie F.The effects of Rosmarinus officinalis essential oil on the
quality changes and fatty acids of Ctenopharyngodon idella. Iran J Fish Sci. 2019;18(1):95–109.
Fu Y, Zu Y, Chen L, et al. Antimicrobial activity of clove and rosemary essential oils alone and in combination. Phyther Res. 2007;21(10):989–994.
Mahapatra AK, Muthukumarappan K, Julson JL. Applications of Ozone, Bacteriocins and Irradiation in Food Processing: A Review. Crit Rev Food Sci Nutr. 2005;45(6):447–461.
Raeisi M, Tajik H, Aminzare M, et al. The Role of Nisin, Monolaurin, and EDTA in Antibacterial Effect of Rosmarinus Officinalis L. and Cinnamomum Zeylanicum Blume Essential Oils on Foodborne Pathogens. J Essent Oil Bear Plants.2016;19(7):1709–1720.
Gao M, Feng L, Jiang T, et al. The use of rosemary extract in combination with nisin to extend the shelf life of pompano (Trachinotus ovatus) fillet during chilled storage. Food Control. 2014;37(1):1–8.
Turgis M, Vu KD, Dupont C, Lacroix M. Combined antimicrobial effect of essential oils and bacteriocins against food-borne pathogens and food spoilage bacteria. Food Res Int. 2012;48(2):696–702.
Dimitrijević SI, Mihajlovski KR, Antonović DG, Milanović-Stevanović MR, Mijin DŽ. A study of the synergistic antilisterial effects of a sub-lethal dose of lactic acid and essential oils from Thymus vulgaris L., Rosmarinus officinalis L., and Origanum vulgare L. Food Chem. 2007;104(2):774–782.
Iseppi R, Camellini S, Sabia C, Messi P. Combined antimicrobial use of essential oils and bacteriocin bacLP17 as seafood biopreservative to control Listeria monocytogenes both in planktonic and in sessile forms. Res Microbiol. 2020;171(8):351–356.
Olasupo NA, Fitzgerald DJ, Narbad A, Gasson MJ. Inhibition of Bacillus subtilis and Listeria innocua by nisin in combination with some naturally occurring organic compounds. J Food Prot. 2004;67(3):596–600.
Cobo Molinos A, Abriouel H, López RL, Omar N Ben, Valdivia E, Gálvez A. Enhanced bactericidal activity of enterocin AS-48 in combination with essential oils, natural bioactive compounds and chemical preservatives against Listeria monocytogenes in ready-to-eat salad. Food Chem Toxicol. 2009;47(9):2216–2223.
Singh B, Bernadette Falahee M, Adams MR. Synergistic inhibition of Listeria monocytogenes by nisin and garlic extract. Food Microbiol. 2001;18(2):133–139.