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Effects of Cell Free Supernatants of Lactobacillus reuteri ATCC55730 and Lactobacillus plantarum FI8595 Against Selected Food-Borne Pathogens and Fish Spoilage Microorganisms

Year 2020, Issue: 20, 485 - 489, 31.12.2020
https://doi.org/10.31590/ejosat.768006

Abstract

The effects of cell free supernatants of Lactobacillus reuteri ATCC55730 and Lactobacillus plantarum FI8595 against selected fish spoilage and food-borne pathogen microorganisms were investigated. For detection of the antimicrobial effect of cell free supernatants from two Lactobacillus strains, four food-borne pathogens (Salmonella Paratyphi A NCTC13, Staphylococcus aureus ATCC29213, Klebsiella pneumoniae ATCC700603, and Listeria monocytogenes ATCC19112) and three fish spoilage bacteria (Proteus mirabilis, Enterococcus faecalis and Pseudomonas luteola) were used. The agar well diffusion method was performed to determine the antimicrobial effects. The cell free supernatants of both L. reuteri and L. plantarum were effective on fish spoilage bacteria tested. Especially, E. faecalis showed high sensitivity against both CFS obtained from L. plantarum and L. reuteri with 16.75 and 22.75 mm inhibition zone diameter, respectively. The CFS of L. reuteri exerted a strong ability to inhibit the growth of all food-borne pathogens. The highest antibacterial effect of CFE of L. reuteri was observed on S. aureus, with the diameter of 26.50 mm inhibition zone.

Supporting Institution

Çukurova Üniversitesi

Thanks

Acknowledge This study was supported by Cukurova University for Department of Scientific Research Projects. The author thanks the Department of Scientific Research Projects at Cukurova University for supporting this study.

References

  • Arena, M. P., Silvain, A., Normanno, G., Grieco, F., Drider, D., Spano, G., & Fiocco, D. (2016). Use of Lactobacillus plantarum strains as a bio-control strategy against food-borne pathogenic microorganisms. Frontiers in microbiology, 7, 464.
  • Arqués, J. L., Fernández, J., Gaya, P., Nuñez, M., Rodrı́guez, E., & Medina, M. (2004). Antimicrobial activity of reuterin in combination with nisin against food-borne pathogens. International Journal of Food Microbiology, 95(2), 225-229.
  • Axelsson LT, Chung TC, Dobrogosz WJ, Lindgren SE (1989) Production of a broad spectrum antimicrobial substance by Lactobacillus reuteri. Microb Ecol Health Dis 2:131–136
  • Basso, A. L., Pıcarıello, G., Coppola, R., Tremonte, P., Musso, S. S., & Luccıa, A. D. (2004). Proteolytic activity of Lactobacillus sakei, Lactobacillus farciminis and Lactobacillus plantarum on sarcoplasmic proteins of pork lean. Journal of food biochemistry, 28(3), 195-212.
  • Bian, L., Molan, A. L., Maddox, I., & Shu, Q. (2011). Antimicrobial activity of Lactobacillus reuteri DPC16 supernatants against selected food borne pathogens. World Journal of Microbiology and Biotechnology, 27(4), 991-998.
  • Corsetti, A., Gobbetti, M., Rossi, J., & Damiani, P. (1998). Antimould activity of sourdough lactic acid bacteria: identification of a mixture of organic acids produced by Lactobacillus sanfrancisco CB1. Applied microbiology and biotechnology, 50(2), 253-256.
  • Cortés-Zavaleta, O., López-Malo, A., Hernández-Mendoza, A., & García, H. S. (2014). Antifungal activity of lactobacilli and its relationship with 3-phenyllactic acid production. International journal of food microbiology, 173, 30-35.
  • Forestier, C., De Champs, C., Vatoux, C., & Joly, B. (2001). Probiotic activities of Lactobacillus casei rhamnosus: in vitro adherence to intestinal cells and antimicrobial properties. Research in Microbiology, 152(2), 167-173.
  • Hassoun, A., & Karoui, R. (2016). Monitoring changes in whiting (Merlangius merlangus) fillets stored under modified atmosphere packaging by front face fluorescence spectroscopy and instrumental techniques. Food Chemistry, 200, 343–353.
  • Hwanhlem N, Ivanova T, Haertlé T, Jaffrès E, Dousset X. Inhibition of food-spoilage and foodborne pathogenic bacteria by a nisin Z-producing Lactococcus lactis subsp lactis KT2W2L. Lwt-Food Sci Technol, 82, 170-175 (2017).
  • Jose N, Bunt C, Hussain M (2015) Comparison of microbiological and probiotic characteristics of Lactobacilli isolates from dairy food products and animal rumen contents. Microorganisms. 3(2), 198-212
  • Khiralla, G. M., Mohamed, E. A., Farag, A. G., & Elhariry, H. (2015). Antibiofilm effect of Lactobacillus pentosus and Lactobacillus plantarum cell-free supernatants against some bacterial pathogens. Journal of Biotech Research, 6, 86.
  • Kleerebezem, M., Boekhorst, J., van Kranenburg, R., Molenaar, D., Kuipers, O. P., Leer, R., ... & Stiekema, W. (2003). Complete genome sequence of Lactobacillus plantarum WCFS1. Proceedings of the National Academy of Sciences, 100(4), 1990-1995.
  • Kos, B., Beganović, J., Jurašić, L., Švađumović, M., Leboš Pavunc, A., Uroić, K., & Šušković, J. (2011). Coculture-inducible bacteriocin biosynthesis of different probiotic strains by dairy starter culture Lactococcus lactis. Mljekarstvo: časopis za unaprjeđenje proizvodnje i prerade mlijeka, 61(4), 273-282.
  • Leroy, F., & De Vuyst, L. (2004). Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends in Food Science & Technology, 15(2), 67-78.
  • Marianelli, C., Cifani, N., & Pasquali, P. (2010). Evaluation of antimicrobial activity of probiotic bacteria against Salmonella enterica subsp. enterica serovar typhimurium 1344 in a common medium under different environmental conditions. Research in microbiology, 161(8), 673-680.
  • Muhsin, Y. M., Majeed, H. Z., & Shawkat, D. S. (2015). CFS and crude bacteriocin of Lactococcus against growth and biofilm formation for some pathogenic bacteria. Int. J. Curr. Microbiol, 4, 35-42.
  • Neal-McKinney, J. M., Lu, X., Duong, T., Larson, C. L., Call, D. R., Shah, D. H., & Konkel, M. E. (2012). Production of organic acids by probiotic lactobacilli can be used to reduce pathogen load in poultry. PloS one, 7(9), e43928.
  • Niku-Paavola, M.-L., Laitila, A., Mattila-Sandholm, T., & Haikara, A. (1999). New types of antimicrobial compounds produced by Lactobacillus plantarum. Journal of Applied Microbiology, 86, 29–35.
  • Nitisinprasert, S., Nilphai, V., Bunyun, P., Sukyai, P., Doi, K., & Sonomoto, K. (2000). Screening and identification of effective thermotolerant lactic acid bacteria producing antimicrobial activity against Escherichia coli and Salmonella sp. resistant to antibiotics. Agriculture and Natural Resources, 34(3), 387-400.
  • Ozogul, Y., Yuvka, İ., Ucar, Y., Durmus, M., Kösker, A. R., Öz, M., & Ozogul, F. (2017). Evaluation of effects of nanoemulsion based on herb essential oils (rosemary, laurel, thyme and sage) on sensory, chemical and microbiological quality of rainbow trout (Oncorhynchus mykiss) fillets during ice storage. LWT, 75, 677-684.
  • Papadimitriou, K., Pot, B., & Tsakalidou, E. (2015). How microbes adapt to a diversity of food niches. Current Opinion in Food Science, 2, 29-35.
  • Ricciardi, A., Blaiotta, G., Di Cerbo, A., Succi, M., & Aponte, M. (2014). Behaviour of lactic acid bacteria populations in Pecorino di Carmasciano cheese samples submitted to environmental conditions prevailing in the gastrointestinal tract: evaluation by means of a polyphasic approach. International journal of food microbiology, 179, 64-71.
  • Rodríguez-Pazo, N., Vázquez-Araújo, L., Pérez-Rodríguez, N., Cortés-Diéguez, S., & Domínguez, J. M. (2013). Cell-free supernatants obtained from fermentation of cheese whey hydrolyzates and phenylpyruvic acid by Lactobacillus plantarum as a source of antimicrobial compounds, bacteriocins, and natural aromas. Applied biochemistry and biotechnology, 171(4), 1042-1060.
  • Sampels, S. (2015). The effects of processing technologies and preparation on the final quality of fish products. Trends in Food Science & Technology, 44(2), 131-146.
  • Shi, S., Qi, Z., Sheng, T., Tu, J., Shao, Y., & Qi, K. (2019). Antagonistic trait of Lactobacillus reuteri S5 against Salmonella enteritidis and assessment of its potential probiotic characteristics. Microbial Pathogenesis, 137, 103773.
  • Soleimani, N. A., Kermanshahi, R. K., Yakhchali, B., & Sattari, T. N. (2010). Antagonistic activity of probiotic lactobacilli against Staphylococcus aureus isolated from bovine mastitis. African Journal of Microbiology Research, 4(20), 2169-2173.
  • Tejero-Sariñena, S., Barlow, J., Costabile, A., Gibson, G. R., & Rowland, I. (2012). In vitro evaluation of the antimicrobial activity of a range of probiotics against pathogens: evidence for the effects of organic acids. Anaerobe, 18(5), 530-538.
  • Tharmaraj, N., & Shah, N. P. (2009). Antimicrobial effects of probiotics against selected pathogenic and spoilage bacteria in cheese-based dips. International Food Research Journal, 16(1), 261-276.
  • Tremonte, P., Pannella, G., Succi, M., Tipaldi, L., Sturchio, M., Coppola, R., ... & Sorrentino, E. (2017). Antimicrobial activity of Lactobacillus plantarum strains isolated from different environments: a preliminary study.
  • Yazgan, H., Ozogul, Y., & Kuley, E. (2019). Antimicrobial influence of nanoemulsified lemon essential oil and pure lemon essential oil on food-borne pathogens and fish spoilage bacteria. International journal of food microbiology, 306, 108266.
  • Yolmeh, M., Khomeiri, M., & Ahmadi, Z. (2017). Application of mixture design to introduce an optimum cell-free supernatant of multiple-strain mixture (MSM) for Lactobacillus against food-borne pathogens. LWT-Food Science and Technology, 83, 298-304.
  • Zhao, Q., Mutukumira, A., Lee, S. J., Maddox, I., & Shu, Q. (2012). Functional properties of free and encapsulated Lactobacillus reuteri DPC16 during and after passage through a simulated gastrointestinal tract. World Journal of Microbiology and Biotechnology, 28(1), 61-70.

Lactobacillus reuteri ATCC55730 ve Lactobacillus plantarum FI8595 Supernatantlarının Bazı Balık Bozucu ve Gıda Kaynaklı Patojen Bakterilerine Karşı Antimikrobiyal Etkisi

Year 2020, Issue: 20, 485 - 489, 31.12.2020
https://doi.org/10.31590/ejosat.768006

Abstract

Bu çalışmada Lactobacillus reuteri ATCC55730 ve Lactobacillus plantarum FI8595 laktik asit bakterileri tarafından üretilen hücresiz supernatantın seçilen gıda kaynaklı patojen ve balık bozucu bakterilerine karşı antimikrobiyal etkisi araştırıldı. İki Lactobacillus suşundan elde edilen supernatantın antimikrobiyal etkisini belirlemek için, dört gıda kaynaklı patojen (Staphylococcus aureus ATCC29213, Salmonella Paratyphi A NCTC13, Klebsiella pneumoniae ATCC700603 ve Listeria monocytogenes ATCC19112) ve üç balık bozucu bakterisi (Proteus mirabilis, Enterococcus faecalis, Pseudomonas luteola’da) kullanıldı. Supernatantların gıda kaynaklı patojen ve balık bozucu bakterileri üzerindeki antimikrobiyal etkisi agar kuyu difüzyon yöntemine göre belirlenmiştir. L. plantarum ve L. reuteri' nin supernatantı, test edilen balık bozucu bakterilerine karşı güçlü bir antimikrobiyal etkiye sahip olmuştur. Özellikle E. faecalis, L. plantarum ve L. reuteri' den elde edilen supernatanta karşı sırayla 16.75 ve 22.75 mm inhibisyon zon çapı ile yüksek bir hassasiyet göstermiştir. L. reuteri'nin supernatnatı, test edilen tüm gıda kaynaklı patojenlerin inhibisyonunda çok güçlü bir yetenek göstermiştir. Özellikle L. reuteri’den elde edilen supernatant, 26.50 mm inhibisyon çapı ile S. aureus'u inhibe etme kabiliyetinin yüksek olduğunu göstermiştir.

References

  • Arena, M. P., Silvain, A., Normanno, G., Grieco, F., Drider, D., Spano, G., & Fiocco, D. (2016). Use of Lactobacillus plantarum strains as a bio-control strategy against food-borne pathogenic microorganisms. Frontiers in microbiology, 7, 464.
  • Arqués, J. L., Fernández, J., Gaya, P., Nuñez, M., Rodrı́guez, E., & Medina, M. (2004). Antimicrobial activity of reuterin in combination with nisin against food-borne pathogens. International Journal of Food Microbiology, 95(2), 225-229.
  • Axelsson LT, Chung TC, Dobrogosz WJ, Lindgren SE (1989) Production of a broad spectrum antimicrobial substance by Lactobacillus reuteri. Microb Ecol Health Dis 2:131–136
  • Basso, A. L., Pıcarıello, G., Coppola, R., Tremonte, P., Musso, S. S., & Luccıa, A. D. (2004). Proteolytic activity of Lactobacillus sakei, Lactobacillus farciminis and Lactobacillus plantarum on sarcoplasmic proteins of pork lean. Journal of food biochemistry, 28(3), 195-212.
  • Bian, L., Molan, A. L., Maddox, I., & Shu, Q. (2011). Antimicrobial activity of Lactobacillus reuteri DPC16 supernatants against selected food borne pathogens. World Journal of Microbiology and Biotechnology, 27(4), 991-998.
  • Corsetti, A., Gobbetti, M., Rossi, J., & Damiani, P. (1998). Antimould activity of sourdough lactic acid bacteria: identification of a mixture of organic acids produced by Lactobacillus sanfrancisco CB1. Applied microbiology and biotechnology, 50(2), 253-256.
  • Cortés-Zavaleta, O., López-Malo, A., Hernández-Mendoza, A., & García, H. S. (2014). Antifungal activity of lactobacilli and its relationship with 3-phenyllactic acid production. International journal of food microbiology, 173, 30-35.
  • Forestier, C., De Champs, C., Vatoux, C., & Joly, B. (2001). Probiotic activities of Lactobacillus casei rhamnosus: in vitro adherence to intestinal cells and antimicrobial properties. Research in Microbiology, 152(2), 167-173.
  • Hassoun, A., & Karoui, R. (2016). Monitoring changes in whiting (Merlangius merlangus) fillets stored under modified atmosphere packaging by front face fluorescence spectroscopy and instrumental techniques. Food Chemistry, 200, 343–353.
  • Hwanhlem N, Ivanova T, Haertlé T, Jaffrès E, Dousset X. Inhibition of food-spoilage and foodborne pathogenic bacteria by a nisin Z-producing Lactococcus lactis subsp lactis KT2W2L. Lwt-Food Sci Technol, 82, 170-175 (2017).
  • Jose N, Bunt C, Hussain M (2015) Comparison of microbiological and probiotic characteristics of Lactobacilli isolates from dairy food products and animal rumen contents. Microorganisms. 3(2), 198-212
  • Khiralla, G. M., Mohamed, E. A., Farag, A. G., & Elhariry, H. (2015). Antibiofilm effect of Lactobacillus pentosus and Lactobacillus plantarum cell-free supernatants against some bacterial pathogens. Journal of Biotech Research, 6, 86.
  • Kleerebezem, M., Boekhorst, J., van Kranenburg, R., Molenaar, D., Kuipers, O. P., Leer, R., ... & Stiekema, W. (2003). Complete genome sequence of Lactobacillus plantarum WCFS1. Proceedings of the National Academy of Sciences, 100(4), 1990-1995.
  • Kos, B., Beganović, J., Jurašić, L., Švađumović, M., Leboš Pavunc, A., Uroić, K., & Šušković, J. (2011). Coculture-inducible bacteriocin biosynthesis of different probiotic strains by dairy starter culture Lactococcus lactis. Mljekarstvo: časopis za unaprjeđenje proizvodnje i prerade mlijeka, 61(4), 273-282.
  • Leroy, F., & De Vuyst, L. (2004). Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends in Food Science & Technology, 15(2), 67-78.
  • Marianelli, C., Cifani, N., & Pasquali, P. (2010). Evaluation of antimicrobial activity of probiotic bacteria against Salmonella enterica subsp. enterica serovar typhimurium 1344 in a common medium under different environmental conditions. Research in microbiology, 161(8), 673-680.
  • Muhsin, Y. M., Majeed, H. Z., & Shawkat, D. S. (2015). CFS and crude bacteriocin of Lactococcus against growth and biofilm formation for some pathogenic bacteria. Int. J. Curr. Microbiol, 4, 35-42.
  • Neal-McKinney, J. M., Lu, X., Duong, T., Larson, C. L., Call, D. R., Shah, D. H., & Konkel, M. E. (2012). Production of organic acids by probiotic lactobacilli can be used to reduce pathogen load in poultry. PloS one, 7(9), e43928.
  • Niku-Paavola, M.-L., Laitila, A., Mattila-Sandholm, T., & Haikara, A. (1999). New types of antimicrobial compounds produced by Lactobacillus plantarum. Journal of Applied Microbiology, 86, 29–35.
  • Nitisinprasert, S., Nilphai, V., Bunyun, P., Sukyai, P., Doi, K., & Sonomoto, K. (2000). Screening and identification of effective thermotolerant lactic acid bacteria producing antimicrobial activity against Escherichia coli and Salmonella sp. resistant to antibiotics. Agriculture and Natural Resources, 34(3), 387-400.
  • Ozogul, Y., Yuvka, İ., Ucar, Y., Durmus, M., Kösker, A. R., Öz, M., & Ozogul, F. (2017). Evaluation of effects of nanoemulsion based on herb essential oils (rosemary, laurel, thyme and sage) on sensory, chemical and microbiological quality of rainbow trout (Oncorhynchus mykiss) fillets during ice storage. LWT, 75, 677-684.
  • Papadimitriou, K., Pot, B., & Tsakalidou, E. (2015). How microbes adapt to a diversity of food niches. Current Opinion in Food Science, 2, 29-35.
  • Ricciardi, A., Blaiotta, G., Di Cerbo, A., Succi, M., & Aponte, M. (2014). Behaviour of lactic acid bacteria populations in Pecorino di Carmasciano cheese samples submitted to environmental conditions prevailing in the gastrointestinal tract: evaluation by means of a polyphasic approach. International journal of food microbiology, 179, 64-71.
  • Rodríguez-Pazo, N., Vázquez-Araújo, L., Pérez-Rodríguez, N., Cortés-Diéguez, S., & Domínguez, J. M. (2013). Cell-free supernatants obtained from fermentation of cheese whey hydrolyzates and phenylpyruvic acid by Lactobacillus plantarum as a source of antimicrobial compounds, bacteriocins, and natural aromas. Applied biochemistry and biotechnology, 171(4), 1042-1060.
  • Sampels, S. (2015). The effects of processing technologies and preparation on the final quality of fish products. Trends in Food Science & Technology, 44(2), 131-146.
  • Shi, S., Qi, Z., Sheng, T., Tu, J., Shao, Y., & Qi, K. (2019). Antagonistic trait of Lactobacillus reuteri S5 against Salmonella enteritidis and assessment of its potential probiotic characteristics. Microbial Pathogenesis, 137, 103773.
  • Soleimani, N. A., Kermanshahi, R. K., Yakhchali, B., & Sattari, T. N. (2010). Antagonistic activity of probiotic lactobacilli against Staphylococcus aureus isolated from bovine mastitis. African Journal of Microbiology Research, 4(20), 2169-2173.
  • Tejero-Sariñena, S., Barlow, J., Costabile, A., Gibson, G. R., & Rowland, I. (2012). In vitro evaluation of the antimicrobial activity of a range of probiotics against pathogens: evidence for the effects of organic acids. Anaerobe, 18(5), 530-538.
  • Tharmaraj, N., & Shah, N. P. (2009). Antimicrobial effects of probiotics against selected pathogenic and spoilage bacteria in cheese-based dips. International Food Research Journal, 16(1), 261-276.
  • Tremonte, P., Pannella, G., Succi, M., Tipaldi, L., Sturchio, M., Coppola, R., ... & Sorrentino, E. (2017). Antimicrobial activity of Lactobacillus plantarum strains isolated from different environments: a preliminary study.
  • Yazgan, H., Ozogul, Y., & Kuley, E. (2019). Antimicrobial influence of nanoemulsified lemon essential oil and pure lemon essential oil on food-borne pathogens and fish spoilage bacteria. International journal of food microbiology, 306, 108266.
  • Yolmeh, M., Khomeiri, M., & Ahmadi, Z. (2017). Application of mixture design to introduce an optimum cell-free supernatant of multiple-strain mixture (MSM) for Lactobacillus against food-borne pathogens. LWT-Food Science and Technology, 83, 298-304.
  • Zhao, Q., Mutukumira, A., Lee, S. J., Maddox, I., & Shu, Q. (2012). Functional properties of free and encapsulated Lactobacillus reuteri DPC16 during and after passage through a simulated gastrointestinal tract. World Journal of Microbiology and Biotechnology, 28(1), 61-70.
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Details

Primary Language English
Subjects Engineering
Journal Section Articles
Authors

Hatice Yazgan 0000-0002-7520-3342

Publication Date December 31, 2020
Published in Issue Year 2020 Issue: 20

Cite

APA Yazgan, H. (2020). Effects of Cell Free Supernatants of Lactobacillus reuteri ATCC55730 and Lactobacillus plantarum FI8595 Against Selected Food-Borne Pathogens and Fish Spoilage Microorganisms. Avrupa Bilim Ve Teknoloji Dergisi(20), 485-489. https://doi.org/10.31590/ejosat.768006