Antibacterial Activity of Plant Extract: the Role of Lemongrass and Chili Extracts, a Bacteriocin from Bacillus velezensis BUU004, and Their Combination to Control Staphylococcus aureus in Dried, Seasoned and Crushed Squid
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Published
Dec 28, 2022
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Abstract
Staphylococcus aureus is the leading cause of foodborne bacterial diseases worldwide, and exists in a wide variety of food products in Thailand, particularly dried seafood products. This study evaluated the inhibitory potential against S. aureus of mixed extracts of lemongrass and hot chili (MLC), bacteriocin, which is produced by Bacillus velezensis BUU004, and their combination, and their effects on physicochemical quality of dried, seasoned, and crushed squids. Dried squid samples were inoculated with S. aureus suspension and then divided into 4 treatments: addition of 1) distilled water (control), 2) a partially-purified solution containing bacteriocin from B. velezensis BUU004 (PPS-BV; 800 AU/mL), 3) an MLC (160 mg/mL), and 4) a combination of the PPS-BV and MLC. Squid samples were maintained at 2 storage temperatures: either at 4°C or room temperature (approximately 25°C) for 28 days. Two administration regimes of the tested additives were applied: a single addition at the onset of the experiment, and a 14-day addition at 14 and 28 days of storage. Strong anti-staphylococcal activity was observed in the dried squids treated with MLC, and a combination of the PPS-BV and MLC during 28-day storage at both conditions, in particular when the 14-day addition was applied. In contrast, the PPS-BV was ineffective against S. aureus in the dried squid samples. The MLC and the combination had bactericidal potency by destroying the bacterial cell walls and cell lysis. Supplementation of the MLC caused a significant reduction (p<0.05) in pH simultaneously with a significant increase (p<0.05) in the water activity of the dried squid during storage. This study suggests a potential use of MLC as a biopreservative for controlling the growth of S. aureus in dried seafood products.
Keywords: Food safety, Seafood, Bacillus, Bacteriocin, Biopreservation
References
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2013.07.004
Al-Hajj, N. Q. M., Algabr, M. N., Raza, H., Thabi, R., Ammar, A. F., Aboshora, W., & Wang, H. (2017). Antibacterial activities of the essential oils of some aromatic medicinal plants to control pathogenic bacteria and extend the shelf-life of seafood. Turkish Journal of Fisheries and Aquatic Sciences, 17, 181-191. https://doi.org/10.4194/1303-2712-v17_1_20
AOAC, (2000). Official method of analysis (17th ed.). Gaithersburg, MD: The Association of Official Analytical Chemists.
Arfatahery, N., Mirshafiey, A., Abedimohtasab, T. P., & Zeinolabedinizamani, M. (2015). Study of the prevalence of Staphylococcus aureus in marine and farmed shrimps in Iran aiming the future development of a prophylactic vaccine. Procedia in Vaccinology, 9, 44-49. https://doi.org/10.
1016/j.provac.2015.05.008
Azizkhani, M., & Tooryan, F. (2015). Antioxidant and antimicrobial activities of rosemary extract, mint extract and a mixture of tocopherols in beef sausage during storage at 4 °C. Journal of Food Safety, 35, 128-136. https://doi.org/10.1111/jfs.12166
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Butkhot, N., Soodsawaeng, P., Samutsan, S., Chotmongcol, K., Vuthiphandchai, V., & Nimrat, S. (2019a). New perspectives for surveying and improving Thai dried seafood qualities using antimicrobials produced by Bacillus velezensis BUU004 against foodborne pathogens. ScienceAsia, 45, 116-126. https://doi.org/10.2306/scienceasia1513-1874.2019.45.116
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Butkhot, N., Soodsawaeng, P., Boonthai, T., Vuthiphandchai, V., & Nimrat, S. (2020). Properties and safety evaluation of Bacillus velezensis BUU004 as probiotic and biopreservative in seafood products. Southeast Asian Journal of Tropical Medicine and Public Health, 51, 201-211.
Castro, A., Silva, J., & Teixeira, P. (2018). Chapter 8: Staphylococcus aureus, a food pathogen: Virulence factors and antibiotic resistance. In A. M. Holban, & A. M. Grumezescu (Eds.), Foodborne Diseases (pp. 213-238). Amsterdam: Elsevier.
Cava-Roda, R., Taboada-Rodríguez, A., López-Gómez, A., Martínez-Hernández, G. B., & Marín-Iniesta, F. (2021). Synergistic antimicrobial activities of combinations of vanillin and essential oils of cinnamon bark, cinnamon leaves and cloves. Foods, 10, 1406. https://doi.org/10.3390/foods10
061406
Field, D., Daly, K., O'Connor, P. M., Cotter, P. D., Hill, C., & Ross, R. P. (2015). Efficacies of nisin A and nisin V semipurified preparations alone and in combination with plant essential oils for controlling Listeria monocytogenes. Applied and Environmental Microbiology, 81, 2762-2769. https://doi.org/
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Hennekinne, J. A., De Buyser, M. L., & Dragacci, S. (2012). Staphylococcus aureus and its food poisoning toxins: Characterization and outbreak investigation. FEMS Microbiology Reviews, 36, 815-836. https://doi.org/10.1111/j.1574-6976.2011.00311.x
Karastogianni, S., Girousi, S., & Sotiropoulos, S. (2016). pH: Principles and measurement. In B. Caballero, P. Finglas, & F. Toldrá (Eds.), The Encyclopedia of Food and Health (pp. 333-338). Oxford: Academic Press.
Kadariya, J., Smith, T. C., & Thapaliya, D. (2014). Staphylococcus aureus and staphylococcal food-borne disease: An ongoing challenge in public health. BioMed Research International, 2014, 827965. http://dx.doi.org/10.1155/2014/827965
Menezes, R. D. P., Bessa, M. A. D. S., Siqueira, C. D. P., Teixeira, S. C., Ferro, E. A. V., Martins, M. M., … Martins, C. H. G. (2022). Antimicrobial, antivirulence, and antiparasitic potential of Capsicum chinense Jacq. extracts and their isolated compound capsaicin. Antibiotics, 11, 1154. https://doi.org/
10.3390/antibiotics11091154
Mukarram, M., Choudhary, S., Khan, M. A., Poltronieri, P., Khan, M. M. A., Ali, J., … Shahid, M. (2022). Lemongrass essential oil components with antimicrobial and anticancer activities. Antioxidants,
11, 20. https://doi.org/ 10.3390/antiox11010020
Nimrat, S., Butkhot, N., Samutsan, S., Chotmongcol, K., Boonthai, T., & Vuthiphandchai, V. (2019). A survey in bacteriological quality of traditional dried seafood products distributed in Chon Buri, Thailand. Science & Technology Asia, 20, 102-114.
Olaimat, A. N., Ghoush, M. A., Al-Holy, M., Hilal, H. A., Al-Nabulsi, A. A., Osaili, T. M., … Holley, R. A. (2021). Survival and growth of Listeria monocytogenes and Staphylococcus aureus in ready-to-eat Mediterranean vegetable salads: Impact of storage temperature and food matrix. International Journal of Food Microbiology, 346, 109149. https://doi.org/10.1016/j.ijfoodmicro.2021.109149
Pato, U., Riftyan, E., Jonnaidi, N. N., Wahyuni, M. S., Feruni, J. A., & Abdel-Wahhab, M. A. (2022). Isolation, characterization, and antimicrobial evaluation of bacteriocin produced by lactic acid bacteria against Erwinia carotovora. Food Science and Technology Campinas, 42, https://doi.org/10.1590/
fst.11922
Saklani, P., Lekshmi, M., Nayak, B. B., & Kumar, S. (2020). Survival of methicillin-resistant Staphylococcus aureus (MRSA) in fish and shrimp at different storage conditions. Journal of Food Protection, 83, 844-848. https://doi.org/10.4315/JFP-19-546
Shahbazi, Y., Shavisi, N., & Mohebi, E. (2016). Effects of Ziziphora clinopodioides essential oil and nisin, both separately and in combination, to extend shelf life and control Escherichia coli O157:H7 and Staphylococcus aureus in raw beef patty during refrigerated storage. Journal of Food Safety, 36, 227-236. https://doi.org/10.1111/jfs.12235
Sikkema, J., Bont, J. A. M., & Poolman, B. (1995). Mechanisms of membrane toxicity of hydrocarbons. Microbiological Reviews, 59, 201-222. https://doi.org/10.1128/mr.59.2.201-222.1995
Simon, S. S., & Sanjeev, S. (2007). Prevalence of enterotoxigenic Staphylococcus aureus in fishery products and fish processing factory workers. Food Control, 18, 1565-1568. https://doi.org/10.1016/j. foodcont.2006.12.007
Soodsawaeng, P., Butkhot, N., Boonthai, T., Vuthiphandchai, V., & Nimrat, S. (2021). Antibacterial activity of bacteriocin produced by Bacillus velezensis BUU004, herb extracts and their combination for controlling spoilage and pathogenic bacteria in dried, seasoned and crushed squid. Srinakharinwirot Science Journal, 37, 1-20.
Soodsawaeng, P., Rattanamangkalanon, N., Boonthai, T., Vuthiphandchai, V., & Nimrat, S. (2022). Preservative potential of Thai herb extracts combined with bacteriocin from Bacillus velezensis BUU004 for controlling food spoilage and pathogenic bacteria in dried crushed seasoned squid. Science & Technology Asia, 27, 74-88.
Tapia, M. S., Alzamora, S. M., & Chirife J. (2020). Effects of water activity (aw) on microbial stability as a hurdle in food preservation. In G. V. Barbosa-Cánovas, A. J. Fontana Jr., S. J. Schmidt, & T. P. Labuza (Eds.), Water Activity in Foods: Fundamentals and Applications 2nd Edition (pp. 323-355). United States: John Wiley & Sons. https://doi.org/10.1002/9781118765982.ch14
Thai Industrial Standards Institute. (2010). Thai industrial standards institute notification (no. 1608), standard of community product (ready-to-eat seasoned squids). Bangkok: Thai Industrial Standards Institute, Ministry of Industry.
Turgis, M., Vu, K. D., Dupont, C., & Lacroix, M. (2012). Combined antimicrobial effect of essential oils and bacteriocins against foodborne pathogens and food spoilage bacteria. Food Research International, 48, 696-702. https://doi.org/10.1016/j.foodres.2012.06.016
US Food Drug Administration. (1998). Bacteriological analytical manual (8th ed.). Gaithersburg, MD: Association of Official Analytical Chemists International.
Weerakkody, N. S., Caffin, N., Dykes, G. A., & Turner, M. S. (2011). Effect of antimicrobial spice and herb extract combinations on Listeria monocytogenes, Staphylococcus aureus, and spoilage microflora growth on cooked ready-to-eat vacuum-packaged shrimp. Journal of Food Protection, 74, 1119-1125. https://doi.org/10.4315/0362-028X.JFP-11-052
Younes, M., Aggett, P., Aguilar, F., Crebelli, R., Dusemund, B, Filipic, M., … Gott, D. (2017). Scientific opinion on the safety of nisin (E 234) as a food additive in the light of new toxicological data and the proposed extension of use. EFSA Journal, 15, 5063. https://doi.org/10.2903/j.efsa.2017.5063
Abdollahzadeh, E., Rezaei, M., & Hosseini, H. (2014). Antibacterial activity of plant essential oils and extracts: The role of thyme essential oil, nisin, and their combination to control Listeria monocytogenes inoculated in minced fish meat. Food Control, 35, 177-183. https://doi.org/10.1016/j.foodcont.
2013.07.004
Al-Hajj, N. Q. M., Algabr, M. N., Raza, H., Thabi, R., Ammar, A. F., Aboshora, W., & Wang, H. (2017). Antibacterial activities of the essential oils of some aromatic medicinal plants to control pathogenic bacteria and extend the shelf-life of seafood. Turkish Journal of Fisheries and Aquatic Sciences, 17, 181-191. https://doi.org/10.4194/1303-2712-v17_1_20
AOAC, (2000). Official method of analysis (17th ed.). Gaithersburg, MD: The Association of Official Analytical Chemists.
Arfatahery, N., Mirshafiey, A., Abedimohtasab, T. P., & Zeinolabedinizamani, M. (2015). Study of the prevalence of Staphylococcus aureus in marine and farmed shrimps in Iran aiming the future development of a prophylactic vaccine. Procedia in Vaccinology, 9, 44-49. https://doi.org/10.
1016/j.provac.2015.05.008
Azizkhani, M., & Tooryan, F. (2015). Antioxidant and antimicrobial activities of rosemary extract, mint extract and a mixture of tocopherols in beef sausage during storage at 4 °C. Journal of Food Safety, 35, 128-136. https://doi.org/10.1111/jfs.12166
Bureau of Epidemiology. (2019). Annual epidemiological surveillance report 2019. Nonthaburi, Thailand: Department of Disease Control, Ministry of Public Health.
Butkhot, N., Soodsawaeng, P., Samutsan, S., Chotmongcol, K., Vuthiphandchai, V., & Nimrat, S. (2019a). New perspectives for surveying and improving Thai dried seafood qualities using antimicrobials produced by Bacillus velezensis BUU004 against foodborne pathogens. ScienceAsia, 45, 116-126. https://doi.org/10.2306/scienceasia1513-1874.2019.45.116
Butkhot, N., Soodsawaeng, P., Vuthiphandchai, V., & Nimrat, S. (2019b). Characterisation and biosafety evaluation of a novel bacteriocin produced by Bacillus velezensis BUU004. International Food Research Journal, 26, 1617-1625.
Butkhot, N., Soodsawaeng, P., Boonthai, T., Vuthiphandchai, V., & Nimrat, S. (2020). Properties and safety evaluation of Bacillus velezensis BUU004 as probiotic and biopreservative in seafood products. Southeast Asian Journal of Tropical Medicine and Public Health, 51, 201-211.
Castro, A., Silva, J., & Teixeira, P. (2018). Chapter 8: Staphylococcus aureus, a food pathogen: Virulence factors and antibiotic resistance. In A. M. Holban, & A. M. Grumezescu (Eds.), Foodborne Diseases (pp. 213-238). Amsterdam: Elsevier.
Cava-Roda, R., Taboada-Rodríguez, A., López-Gómez, A., Martínez-Hernández, G. B., & Marín-Iniesta, F. (2021). Synergistic antimicrobial activities of combinations of vanillin and essential oils of cinnamon bark, cinnamon leaves and cloves. Foods, 10, 1406. https://doi.org/10.3390/foods10
061406
Field, D., Daly, K., O'Connor, P. M., Cotter, P. D., Hill, C., & Ross, R. P. (2015). Efficacies of nisin A and nisin V semipurified preparations alone and in combination with plant essential oils for controlling Listeria monocytogenes. Applied and Environmental Microbiology, 81, 2762-2769. https://doi.org/
10.1128/AEM.00070-15
Fisheries Statistics of Thailand. (2019). Fisheries statistics of Thailand 2017, no. 9/2019. Bangkok, Thailand: Department of Fisheries, Ministry of Agriculture and Cooperatives.
Food Sanitation Division. (2020). Occurrence of food safety at commercial distribution areas in Bangkok. Bangkok: Health Department, Bangkok Metropolitan Administration.
Hennekinne, J. A., De Buyser, M. L., & Dragacci, S. (2012). Staphylococcus aureus and its food poisoning toxins: Characterization and outbreak investigation. FEMS Microbiology Reviews, 36, 815-836. https://doi.org/10.1111/j.1574-6976.2011.00311.x
Karastogianni, S., Girousi, S., & Sotiropoulos, S. (2016). pH: Principles and measurement. In B. Caballero, P. Finglas, & F. Toldrá (Eds.), The Encyclopedia of Food and Health (pp. 333-338). Oxford: Academic Press.
Kadariya, J., Smith, T. C., & Thapaliya, D. (2014). Staphylococcus aureus and staphylococcal food-borne disease: An ongoing challenge in public health. BioMed Research International, 2014, 827965. http://dx.doi.org/10.1155/2014/827965
Menezes, R. D. P., Bessa, M. A. D. S., Siqueira, C. D. P., Teixeira, S. C., Ferro, E. A. V., Martins, M. M., … Martins, C. H. G. (2022). Antimicrobial, antivirulence, and antiparasitic potential of Capsicum chinense Jacq. extracts and their isolated compound capsaicin. Antibiotics, 11, 1154. https://doi.org/
10.3390/antibiotics11091154
Mukarram, M., Choudhary, S., Khan, M. A., Poltronieri, P., Khan, M. M. A., Ali, J., … Shahid, M. (2022). Lemongrass essential oil components with antimicrobial and anticancer activities. Antioxidants,
11, 20. https://doi.org/ 10.3390/antiox11010020
Nimrat, S., Butkhot, N., Samutsan, S., Chotmongcol, K., Boonthai, T., & Vuthiphandchai, V. (2019). A survey in bacteriological quality of traditional dried seafood products distributed in Chon Buri, Thailand. Science & Technology Asia, 20, 102-114.
Olaimat, A. N., Ghoush, M. A., Al-Holy, M., Hilal, H. A., Al-Nabulsi, A. A., Osaili, T. M., … Holley, R. A. (2021). Survival and growth of Listeria monocytogenes and Staphylococcus aureus in ready-to-eat Mediterranean vegetable salads: Impact of storage temperature and food matrix. International Journal of Food Microbiology, 346, 109149. https://doi.org/10.1016/j.ijfoodmicro.2021.109149
Pato, U., Riftyan, E., Jonnaidi, N. N., Wahyuni, M. S., Feruni, J. A., & Abdel-Wahhab, M. A. (2022). Isolation, characterization, and antimicrobial evaluation of bacteriocin produced by lactic acid bacteria against Erwinia carotovora. Food Science and Technology Campinas, 42, https://doi.org/10.1590/
fst.11922
Saklani, P., Lekshmi, M., Nayak, B. B., & Kumar, S. (2020). Survival of methicillin-resistant Staphylococcus aureus (MRSA) in fish and shrimp at different storage conditions. Journal of Food Protection, 83, 844-848. https://doi.org/10.4315/JFP-19-546
Shahbazi, Y., Shavisi, N., & Mohebi, E. (2016). Effects of Ziziphora clinopodioides essential oil and nisin, both separately and in combination, to extend shelf life and control Escherichia coli O157:H7 and Staphylococcus aureus in raw beef patty during refrigerated storage. Journal of Food Safety, 36, 227-236. https://doi.org/10.1111/jfs.12235
Sikkema, J., Bont, J. A. M., & Poolman, B. (1995). Mechanisms of membrane toxicity of hydrocarbons. Microbiological Reviews, 59, 201-222. https://doi.org/10.1128/mr.59.2.201-222.1995
Simon, S. S., & Sanjeev, S. (2007). Prevalence of enterotoxigenic Staphylococcus aureus in fishery products and fish processing factory workers. Food Control, 18, 1565-1568. https://doi.org/10.1016/j. foodcont.2006.12.007
Soodsawaeng, P., Butkhot, N., Boonthai, T., Vuthiphandchai, V., & Nimrat, S. (2021). Antibacterial activity of bacteriocin produced by Bacillus velezensis BUU004, herb extracts and their combination for controlling spoilage and pathogenic bacteria in dried, seasoned and crushed squid. Srinakharinwirot Science Journal, 37, 1-20.
Soodsawaeng, P., Rattanamangkalanon, N., Boonthai, T., Vuthiphandchai, V., & Nimrat, S. (2022). Preservative potential of Thai herb extracts combined with bacteriocin from Bacillus velezensis BUU004 for controlling food spoilage and pathogenic bacteria in dried crushed seasoned squid. Science & Technology Asia, 27, 74-88.
Tapia, M. S., Alzamora, S. M., & Chirife J. (2020). Effects of water activity (aw) on microbial stability as a hurdle in food preservation. In G. V. Barbosa-Cánovas, A. J. Fontana Jr., S. J. Schmidt, & T. P. Labuza (Eds.), Water Activity in Foods: Fundamentals and Applications 2nd Edition (pp. 323-355). United States: John Wiley & Sons. https://doi.org/10.1002/9781118765982.ch14
Thai Industrial Standards Institute. (2010). Thai industrial standards institute notification (no. 1608), standard of community product (ready-to-eat seasoned squids). Bangkok: Thai Industrial Standards Institute, Ministry of Industry.
Turgis, M., Vu, K. D., Dupont, C., & Lacroix, M. (2012). Combined antimicrobial effect of essential oils and bacteriocins against foodborne pathogens and food spoilage bacteria. Food Research International, 48, 696-702. https://doi.org/10.1016/j.foodres.2012.06.016
US Food Drug Administration. (1998). Bacteriological analytical manual (8th ed.). Gaithersburg, MD: Association of Official Analytical Chemists International.
Weerakkody, N. S., Caffin, N., Dykes, G. A., & Turner, M. S. (2011). Effect of antimicrobial spice and herb extract combinations on Listeria monocytogenes, Staphylococcus aureus, and spoilage microflora growth on cooked ready-to-eat vacuum-packaged shrimp. Journal of Food Protection, 74, 1119-1125. https://doi.org/10.4315/0362-028X.JFP-11-052
Younes, M., Aggett, P., Aguilar, F., Crebelli, R., Dusemund, B, Filipic, M., … Gott, D. (2017). Scientific opinion on the safety of nisin (E 234) as a food additive in the light of new toxicological data and the proposed extension of use. EFSA Journal, 15, 5063. https://doi.org/10.2903/j.efsa.2017.5063
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How to Cite
SOODSAWAENG, Pornpimon et al.
Antibacterial Activity of Plant Extract: the Role of Lemongrass and Chili Extracts, a Bacteriocin from Bacillus velezensis BUU004, and Their Combination to Control Staphylococcus aureus in Dried, Seasoned and Crushed Squid.
Naresuan University Journal: Science and Technology (NUJST), [S.l.], v. 31, n. 1, p. 93-106, dec. 2022.
ISSN 2539-553X.
Available at: <https://www.journal.nu.ac.th/NUJST/article/view/Vol-31-No-1-2023-93-106>. Date accessed: 27 apr. 2024.
doi: https://doi.org/10.14456/nujst.2023.10.