The effect of low temperatures and osmotic stress on the growth of lactic acid bacteria

Keywords: fish products, lactic acid bacteria, Latilactobacillus sakei, sodium chloride, osmotic stress, salt stress, low temperatures

Abstract

Background. To date, the use of lactic acid bacteria has not found wide industrial application in the production of fish products. At the same time, the scientific direction associated with the development and use of bacterial cultures for the processing of fish products is highly relevant. Technological processes of fish processing often involve the use of high concentrations of NaCl and low positive temperatures; these factors inhibit the growth and development of most microorganisms. Therefore, the development of bacterial cultures to produce fish products should include the study of tolerance of probiotic strains to these stress factors. Latilactobacillus sakei species have great prospects for the use as bacterial cultures for fish products processing due to high biochemical activity and potential probiotic properties.

Purpose. The aim of the study was to study the resistance of Latilactobacillus sakei strains to high sodium chloride concentrations and low temperatures. The objects of the study were four strains of Latilactobacillus sakei.

Materials and methods. Cultivation of lactic acid bacteria was carried out on MRS medium at a temperature of 37 °C. The ability of bacteria to grow in the presence of sodium chloride was determined on MRS medium containing 12% NaCl, and the tolerance of bacteria to low positive temperatures was studied by strains cultivation at 8 °C.

Results. As a result of the studies, it was proven that the strains Llb. sakei LSK-45, Llb. sakei LSK-104, Llb. sakei LSK-103 can grow in the medium with a high concentration of NaCl (12%) and at low positive temperatures.

Conclusion. Thus, the use of Llb. sakei LSK-45, Llb. sakei LSK-104, Llb. sakei LSK-103 strains in the fish processing industry is of great scientific interest.

EDN: ECLXVD

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Author Biographies

Anna P. Nikiforova, ITMO University

Cand. Sci. (Technology), Associate Professor of the Faculty of Biotechnologies

Irina S. Khamagaeva, East Siberia State University of Technology and Management

Dr. Sci. (Technology), Professor

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Hossain, M.I. et al. (2021). Comprehensive molecular, probiotic, and quorum-sensing characterization of anti-listerial lactic acid bacteria, and application as bioprotective in a food (milk) model. Journal of Dairy Science, 104(6), 6516-6534. https://doi.org/10.3168/jds.2020-19034 EDN: https://elibrary.ru/dwfyde

Kim, H.S., Oh, H., Kim, B. et al. (2023). Multifunctional effects of Lactobacillus sakei HEM 224 on the gastrointestinal tract and airway inflammation. Scientific Reports, 13, 17918. https://doi.org/10.1038/s41598-023-45043-0 EDN: https://elibrary.ru/cpgcrn

Liu, S., Ma, Y., Zheng, Y., Zhao, W., Zhao, X., Luo, T., Zhang, J. & Yang, Z. (2020). Cold-Stress Response of Probiotic Lactobacillus plantarum K25 by iTRAQ Proteomic Analysis. Journal of Microbiology and Biotechnology, 30(2), 187-195. https://doi.org/10.4014/jmb.1909.09021 EDN: https://elibrary.ru/slpyzn

Marceau, A., Zagorec, M. & Champomier-Vergès, M.C. (2003). Positive effects of growth at suboptimal temperature and high salt concentration on long-term survival of Lactobacillus sakei. Research in Microbiology, 154, 37-42. https://doi.org/10.1016/S0923-2508(02)00010-4

Miller, M.B. (2001). Quorum sensing in bacteria. Annual Review of Microbiology, 55, 165-199. https://doi.org/10.1146/annurev.micro.55.1.165

Montanari, C., Barbieri, F., Magnani, M., Grazia, L., Gardini, F. & Tabanelli, G. (2018). Phenotypic Diversity of Lactobacillus sakei Strains. Frontiers in Microbiology, 9. https://doi.org/10.3389/fmicb.2018.02003

Nikiforova, A., Zamaratskaia, G. & Pickova, J. (2020). Fatty acid composition of salted and fermented products from Baikal omul (Coregonus autumnalis migratorius). Journal of Food Science and Technology, 57, 595-605. https://doi.org/10.1007/s13197-019-04091-z EDN: https://elibrary.ru/zmeach

Qian, X., Tian, P., Zhao, J., Zhang, H., Wang, G. & Chen, W. (2022). Quorum Sensing of Lactic Acid Bacteria: Progress and Insights. Food Reviews International, 39(7), 4781-4792. https://doi.org/10.1080/87559129.2022.2062766 EDN: https://elibrary.ru/mhdkzq

Skåra, T., Axelsson, L., Stefansson, G., Ekstrand, B. & Hagen, H. (2015). Fermented and ripened fish products in the northern European countries. Journal of Ethnic Foods, 2(1), 18-24. https://doi.org/10.1016/j.jef.2015.02.004

Song, E.J., Lee, E.S., Park, S.L., Choi, H.J., Roh, S.W. & Nam, Y.D. (2018). Bacterial community analysis in three types of the fermented seafood, jeotgal, produced in South Korea. Bioscience, Biotechnology and Biochemistry, 82(8), 1444-1454. https://doi.org/10.1080/09168451.2018.1469395

Speranza, B., Racioppo, A., Bevilacqua, A., Beneduce, L., Sinigaglia, M. & Corbo, M.R. (2015). Selection of Autochthonous Strains as Starter Cultures for Fermented Fish Products. Journal of Food Science, 80(1), M151-M160. https://doi.org/10.1111/1750-3841.12721

Tajdozian, H., Seo, H., Jeong, Y. et al. (2024). Efficacy of lyophilized Lactobacillus sakei as a potential candidate for preventing carbapenem-resistant Klebsiella infection. Annals of Microbiology, 74(28). https://doi.org/10.1186/s13213-024-01773-8 EDN: https://elibrary.ru/ywbksc

Trunk, T., Khalil, H.S. & Leo, J.C. (2018). Bacterial autoaggregation. AIMS Microbiology, 4(1), 140-164. https://doi.org/10.3934/microbiol.2018.1.140

Yang, H., He, M. & Wu, C. (2021). Cross protection of lactic acid bacteria during environmental stresses: Stress responses and underlying mechanisms. LWT, 144, 111203. https://doi.org/10.1016/j.lwt.2021.111203 EDN: https://elibrary.ru/nvykru

Zagorec, M. & Champomier-Vergès, M.C. (2017). Lactobacillus sakei: A Starter for Sausage Fermentation, a Protective Culture for Meat Products. Microorganisms, 5(3), 56. https://doi.org/10.3390/microorganisms5030056

Zou, X., Pan, L., Xu, M., Wang, X., Wang, Q. & Han, Y. (2023). Probiotic potential of Lactobacillus sakei L-7 in regulating gut microbiota and metabolism. Microbiological Research, 274, 127438. https://doi.org/10.1016/j.micres.2023.127438 EDN: https://elibrary.ru/dbxzls

References

Nikiforova, A.P., Khazagaeva, S.N. & Artyukhova, S.I. (2019). Research of biochemical activity of Lactobacillus sakei LSK-104 strain. Vestnik VSGUTU, 4(75), 62-68. EDN: https://elibrary.ru/arivmh

Nikiforova, A.P. (2020). Prospects for the production of fermented fish products using lactic acid bacteria. Technologies of Food and Processing Industry of Agro-Industrial Complex — Healthy Food Products, 2, 17-24. https://doi.org/10.24411/2311-6447-2020-10038 EDN: https://elibrary.ru/zejayp

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Ammor, S., Dufour, E., Zagorec, M., Chaillou, S. & Chevallier, I. (2005). Characterization and selection of Lactobacillus sakei strains isolated from traditional dry-sausage. Food Microbiology, 22, 529-538. https://doi.org/10.1016/j.fm.2004.11.016

Bonaccio, M., Ruggiero, E., Castelnuovo, A.D., Costanzo, S., Persichillo, M., Curtis, A.D. & Iacoviello, L. (2017). Fish intake is associated with lower cardiovascular risk in a Mediterranean population: Prospective results from the Molisani study. Nutrition, Metabolism and Cardiovascular Diseases, 27, 865-873. https://doi.org/10.1016/j.numecd.2017.08.004

Chai, H.J., Wu, C.J., Yang, S.H., Li, T.L. & Pan, B.S. (2016). Peptides from hydrolysate of lantern fish (Benthosema pterotum) proved neuroprotective in vitro and in vivo. Journal of Functional Foods, 24, 438-449. https://doi.org/10.1016/j.jff.2016.04.009

Chaillou, S., Champomier-Vergès, M.C., Cornet, M., Crutz Le Coq, A.M., Dudzé, A.M., Martin, V., Beaufils, S., Bossy, R., Darbon-Rongère, E., Loux, V. et al. (2005). Complete genome sequence of the meat-borne lactic acid bacterium Lactobacillus sakei 23K. Nature Biotechnology, 23, 1527-1533. https://doi.org/10.1038/nbt1160

Chen, J., Jayachandran, M., Bai, W. & Xu, B. (2022). A critical review on the health benefits of fish consumption and its bioactive constituents. Food Chemistry, 369, 130874. https://doi.org/10.1016/j.foodchem.2021.130874 EDN: https://elibrary.ru/fjsqlf

Gao, X., Kong, J., Zhu, H., Mao, B., Cui, S. & Zhao, J. (2022). Lactobacillus, Bifidobacterium and Lactococcus response to environmental stress: Mechanisms and application of cross-protection to improve resistance against freeze-drying. Journal of Applied Microbiology, 132, 802-821. https://doi.org/10.1111/jam.15251 EDN: https://elibrary.ru/hezagp

Gu, Y., Li, B., Tian, J., Wu, R. & He, Y. (2018). The response of LuxS/AI-2 quorum sensing in Lactobacillus fermentum 2-1 to changes in environmental growth conditions. Annals of Microbiology, 68, 287-294. https://doi.org/10.1007/s13213-018-1337-z EDN: https://elibrary.ru/llqblr

Van de Guchte, M., Serror, P., Chervaux, C., Smokvina, T., Ehrlich, S.D. & Maguin, E. (2002). Stress responses in lactic acid bacteria. Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology, 82(1-4), 187-216. https://doi.org/10.1023/A:1020631532202 EDN: https://elibrary.ru/mcgexh

Hossain, M.I. et al. (2021). Comprehensive molecular, probiotic, and quorum-sensing characterization of anti-listerial lactic acid bacteria, and application as bioprotective in a food (milk) model. Journal of Dairy Science, 104(6), 6516-6534. https://doi.org/10.3168/jds.2020-19034 EDN: https://elibrary.ru/dwfyde

Kim, H.S., Oh, H., Kim, B. et al. (2023). Multifunctional effects of Lactobacillus sakei HEM 224 on the gastrointestinal tract and airway inflammation. Scientific Reports, 13, 17918. https://doi.org/10.1038/s41598-023-45043-0 EDN: https://elibrary.ru/cpgcrn

Liu, S., Ma, Y., Zheng, Y., Zhao, W., Zhao, X., Luo, T., Zhang, J. & Yang, Z. (2020). Cold-Stress Response of Probiotic Lactobacillus plantarum K25 by iTRAQ Proteomic Analysis. Journal of Microbiology and Biotechnology, 30(2), 187-195. https://doi.org/10.4014/jmb.1909.09021 EDN: https://elibrary.ru/slpyzn

Marceau, A., Zagorec, M. & Champomier-Vergès, M.C. (2003). Positive effects of growth at suboptimal temperature and high salt concentration on long-term survival of Lactobacillus sakei. Research in Microbiology, 154, 37-42. https://doi.org/10.1016/S0923-2508(02)00010-4

Miller, M.B. (2001). Quorum sensing in bacteria. Annual Review of Microbiology, 55, 165-199. https://doi.org/10.1146/annurev.micro.55.1.165

Montanari, C., Barbieri, F., Magnani, M., Grazia, L., Gardini, F. & Tabanelli, G. (2018). Phenotypic Diversity of Lactobacillus sakei Strains. Frontiers in Microbiology, 9. https://doi.org/10.3389/fmicb.2018.02003

Nikiforova, A., Zamaratskaia, G. & Pickova, J. (2020). Fatty acid composition of salted and fermented products from Baikal omul (Coregonus autumnalis migratorius). Journal of Food Science and Technology, 57, 595-605. https://doi.org/10.1007/s13197-019-04091-z EDN: https://elibrary.ru/zmeach

Qian, X., Tian, P., Zhao, J., Zhang, H., Wang, G. & Chen, W. (2022). Quorum Sensing of Lactic Acid Bacteria: Progress and Insights. Food Reviews International, 39(7), 4781-4792. https://doi.org/10.1080/87559129.2022.2062766 EDN: https://elibrary.ru/mhdkzq

Skåra, T., Axelsson, L., Stefansson, G., Ekstrand, B. & Hagen, H. (2015). Fermented and ripened fish products in the northern European countries. Journal of Ethnic Foods, 2(1), 18-24. https://doi.org/10.1016/j.jef.2015.02.004

Song, E.J., Lee, E.S., Park, S.L., Choi, H.J., Roh, S.W. & Nam, Y.D. (2018). Bacterial community analysis in three types of the fermented seafood, jeotgal, produced in South Korea. Bioscience, Biotechnology and Biochemistry, 82(8), 1444-1454. https://doi.org/10.1080/09168451.2018.1469395

Speranza, B., Racioppo, A., Bevilacqua, A., Beneduce, L., Sinigaglia, M. & Corbo, M.R. (2015). Selection of Autochthonous Strains as Starter Cultures for Fermented Fish Products. Journal of Food Science, 80(1), M151-M160. https://doi.org/10.1111/1750-3841.12721

Tajdozian, H., Seo, H., Jeong, Y. et al. (2024). Efficacy of lyophilized Lactobacillus sakei as a potential candidate for preventing carbapenem-resistant Klebsiella infection. Annals of Microbiology, 74(28). https://doi.org/10.1186/s13213-024-01773-8 EDN: https://elibrary.ru/ywbksc

Trunk, T., Khalil, H.S. & Leo, J.C. (2018). Bacterial autoaggregation. AIMS Microbiology, 4(1), 140-164. https://doi.org/10.3934/microbiol.2018.1.140

Yang, H., He, M. & Wu, C. (2021). Cross protection of lactic acid bacteria during environmental stresses: Stress responses and underlying mechanisms. LWT, 144, 111203. https://doi.org/10.1016/j.lwt.2021.111203 EDN: https://elibrary.ru/nvykru

Zagorec, M. & Champomier-Vergès, M.C. (2017). Lactobacillus sakei: A Starter for Sausage Fermentation, a Protective Culture for Meat Products. Microorganisms, 5(3), 56. https://doi.org/10.3390/microorganisms5030056

Zou, X., Pan, L., Xu, M., Wang, X., Wang, Q. & Han, Y. (2023). Probiotic potential of Lactobacillus sakei L-7 in regulating gut microbiota and metabolism. Microbiological Research, 274, 127438. https://doi.org/10.1016/j.micres.2023.127438 EDN: https://elibrary.ru/dbxzls


Published
2025-08-31
How to Cite
Nikiforova, A., & Khamagaeva, I. (2025). The effect of low temperatures and osmotic stress on the growth of lactic acid bacteria. Siberian Journal of Life Sciences and Agriculture, 17(3), 169-187. https://doi.org/10.12731/2658-6649-2025-17-3-1244
Section
Biochemistry, Genetics and Molecular Biology