Selenium accumulation by Lactobacillus isolated from commercial fermented milk: minimum inhibitory concentration and kinetic growth changes

  • A. Castañeda-Ovando
  • E. Pérez-Escalante
  • G.M. Rodríguez-Serrano
  • X. Martínez-Ramírez
  • E. Contreras-López
  • J. Jaimez-Ordaz
  • J. Añorve-Morga
  • S. Nieto-Velázquez
  • J. Ramírez-Godínez
  • L.G. González Olivares
Keywords: Selenium, probiotic, lactobacillus, selenoamino acid, selenocysteine

Abstract

Selenium is essential for human health; however, recommended daily intake is not always met. Thus, studies have been carried out on the biogenic production of more bioavailable selenium. It has been demonstrated that certain lactobacilli can metabolize inorganic selenium to transform it into selenoamino acids. This study aimed to add selenium on  Lactobacillus casei Shirota and Lactobacillus johnsonii La1, isolated from commercial dairy products through an MRS media fermentation enriched with Na2SeO3 to determine the minimum inhibitory concentration, the changes in the kinetics growth, and the selenium bioaccumulation. The minimum inhibitory concentration (MIC) was determined using the Talmadge and Fitch method. Kinetic changes were calculated by modeling the growth curve, and an inductively coupled plasma (ICP) assay was used to determine selenium accumulation by the cell. The MIC of Na2SeO3 was higher than 190 mg/L in both bacteria, and kinetic changes showed faster growth when media was not enriched. Selenium absorption of 64.50 % was found for Lb. casei Shirota and 75.78 % for Lb. johnsonii La1. Obtained results demonstrated that these lactic acid bacteria bacteria are a potential ingredient in functional food processing to their ability to accumulate selenium.

References

Alzate, A., Fernandez-Fernández, A, Pérez-Conde, M. C., Gutierrez, A. M. and Cámara, C. (2008). Comparison of biotransformation of inorganic selenium by Lactobacillus and Saccharomyces in lactic fermentation process of yogurt and kefir. Journal of Agricultural and Food Chemistry 56, 8728–8736. https://doi.org/10.1021/jf8013519

Alzate, A., Perez-Conde, M. C., Gutiérrez, A. M. and Camara C. (2010). Selenium-enriched' fermented milk: A suitable dairy product to improve selenium intake in humans. International Dairy Journal 20, 761–769. https://doi.org/10.1016/j.idairyj.2010.05.007

Amit, K., Sravani, T., Mohd, A. S, Pooladanda, V. and Chandraiah, G. (2019). Therapeutic applications of selenium nanoparticles. Biomedicine and Pharmacotherapy 111, 802–812. https://doi.org/10.1016/j.biopha.2018.12.146.

Andreoni, V., Moro-Luischi, M., Cavalca, L., Erba, D. and Ciappellano, S. (2000). Selenite tolerance and accumulation in the Lactobacillus species. Annals of Microbiology 50, 77–88.

Castañeda-Ovando, A., Segovia-Cruz, J. A., Flores-Aguilar, J. F., Rodríguez-Serrano, G. M., Salazar-Pereda, V., Ramírez-Godínez, J., Contreras-López, E., Jaimez-Ordaz, J. and González-Olivares, L. G. (2019). Serine-enriched minimal medium enhances conversion of selenium into selenocysteine by Streptococcus thermophilus. Journal of Dairy Science 102, 6781–6789, https://doi.org/10.3168/jds.2019-16365.

Ceja-Medina, L. I., Medina-Torres, L., González-Ávila, M., Martínez-Rodríguez, J. C., Andrade-González, I., Calderón-Santoyo, M. and Ortíz-Basurto, R. I. (2021). In-vitro symbiotic activity of Lactobacillus plantarum encapsulated with mixtures of Aloe vera mucilage, agave fructans and food aditives as wall materials. Revista Mexicana de Ingeniería Química 20(2), 711–723. https://doi.org/10.24275/rmiq/Bio2234

Chen, Y., Li, Q., Xia, C., Yang, F., Xu, N., Wu, Q., Hu, Y., Xia, L., Wang, C. and Zhou, M. (2019). Effect of selenium supplements on the antioxidant activity and nitrite degradation of lactic acid bacteria. World Journal of Microbiology and Biotechnology 35,61. https://doi.org/10.1007/s11274-019-2609-x

Crespo, L., Gaglio, R., Martínez, F. G., Moreno-Martin, G., Franciosi, E., Madrid-Albarrán, Luca-Settanni, Y., Mozzi, F. and Pescuma, M. (2021). Bioaccumulation of selenium-by fruit origin lactic acid bacteria in tropical fermented fruit juices. LWT 151, 112103. https://doi.org/10.1016/j.lwt.2021.112103

Cruz, L. Y., Wang, D. and Liu, J. (2018). Biosynthesis of selenium nanoparticles, characterization and X-ray induced radiotherapy for the treatment of lung cancer with interstitial lung disease, J Photochemistry and Photobiology 191,123–127, https://doi.org/10.1016/j.jphotobiol.2018.12.008.

Escobar-Ramírez, M. C., Castañeda-Ovando, A., Pérez-Escalante, E., Rodríguez-Serrano, G. M., Ramírez-Moreno, E., Quintero-Lira, A., Contreras-López, E., Añorve-Morga, J., Jaimez-Ordaz, J. and González-Olivares, L. G. (2021). Antimicrobial activity of Se-nanoparticles from bacterial biotransformation. Fermentation 7, 130, https://doi.org/10.3390/fermentation7030130

Ferreira, R. L. U., Sena-Evangelista, K. C. M., de Azevedo, E. P., Pinheiro, F. I,. Cobucci, R. N. and Campos-Pedrosa, L.F. (2021). Selenium in human health and gut microflora: Bioavailability of selenocompounds and relationship with diseases. Frontiers in Nutrition 8, 685317. https://doi.org/10.3389/fnut.2021.685317.

Gangadoo, S., Dinev, I., Willson, N. L., Moore, R. J., Chapman, J. and Stanley, D. (2020). Nanoparticles of selenium as high bioavailable and non-toxic supplement alternatives for broiler chickens. Environmental Science and Pollution Research. 27, 16159–16166. https://doi.org/10.1007/s11356-020-07962-7

Gheorghiu, M. L. and Badiu, C. (2020). Selenium involvement in mitochondrial function in thyroid disorders. Hormones 19, 25–30. https://doi.org/10.1007/s42000-020-00173-2

González-Olivares, L. G., Contreras-López, E., Flores-Aguilar, J. F., Rodríguez-Serrano, G. M., Castañeda-Ovando, A., Jaimez-Ordaz, J., Añorve-Morga, J. and Cruz-Guerrero, A. E. (2016). Inorganic selenium uptake by Lactobacillus ssp. Revista Mexicana de Ingeniería Quimica 15, 33–38. http://www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S1665-27382016000100033

Kousha, M., Yeganeh, S. and Keramat-Amirkolaie, A. (2017). Effect of sodium selenite on the bacteria growth, selenium accumulation, and selenium biotransformation in Pediococcus acidilactici. Food Science and Biotechnology. 26, 1013–1018. https://doi.org/10.1007/s10068-017-0142-y

Krausova, G., Kana, A., Hyrslova, I., Mrvikova, I and Kavkova, M. (2020). Development of selenized lactic acid bacteria and their selenium bioaccummulation capacity. Fermentation 6, 91. https://doi.org/10.3390/fermentation6030091

Ibrahim, S. A. Z., Kerkadi, A. and Agouni, A. (2019). Selenium and health: An updateon the situation in the middle east and north Africa. Nutrients 11, 1457, https://doi.org/10.3390/nu11071457

Martínez, F. G., Cuencas-Barrientos, M. E., Mozzi, F. and Pescuma, M. (2019). Survival of selenium-enriched lactic acid bacteria in a fermented drink under storage and simulated gastrointestinal digestion. Food Research International 123, 115–124, https://doi.org/10.1016/j.foodres.2019.04.057

Martínez, F. G., Moreno-Martin, G., Pescuma, M., Madrid-Albarrán, Y. and Mozzi, F. (2020). Biotransformation of selenium by lactic acid bacteria: Formation of seleno-nanoparticles and seleno-amino acids. Frontiers in Bioengineering and Biotechnology 8, 506. http://doi.org/10.3389/fbioe.2020.00506

Martínez-Preciado, A. H., Silva-Jara, J. M., Flores-Nuño, B. A., Michel, C. R., Castellanos-Haro, A., & Macías-Rodríguez, M. E. (2021). Microencapsulation by spray-drying of Manilkara zapota pulp and probiotics (Lactobacillus fermentum A15): Assessment of shelf-life in a food matrix. Revista Mexicana de Ingeniería Química, 20(2), 635-648.

Mrvčić, J., Stanzer, D., Šolić, E. and Stehlik-Thomas, V. (2012). Interaction of lactic acid bacteria with metal ions: opportunities for improving food safety and quality. World Journal of Microbiology and Biotechnology 28, 2771–2782. https://doi.org/10.1007/s11274-012-1094-2

Peña, R. and Circo, S. (2007). Solución automatica del método de Talmage y Fitch. Tecnología Química. 27, 10–15.

Pham, H. D., Siddik, M. A. B., Fotedar, R., Nguyen, C. M., Nahar, A. and Gupta, S. K. (2019). Total bioavailable organic selenium in fishmeal-based diet influences growth and physiology of juvenile cobia Rachycentron canadum (Linnaeus, 1766). Biological Trace Elements Research 190, 541–549. https://doi.org/10.1007/s12011-018-1565-x

Pieniz, S., Andreazza, R., Mann, M. B., Camargo, F. and Brandelli, A. (2016). Bioaccumulation and distribution of selenium in Enterococcus durans. Journal of Trace Elements in Medicine and Biology 40, 37–45. https://doi.org/10.1016/j.jtemb.2016.12.003

Pophaly, S. D., Poonam, Singh, P., Kumar, H., Tomar, S. K. and Singh, R. (2014). Selenium enrichment of lactic acid bacteria and bifidobacteria: A functional food perspective. Trends in Food Science and Technology. 39, 135–145. https://doi.org/10.1016/j.tifs.2014.07.006.

Pusztahelyi, T., Kovács, S., Pócsi, I. and Prokisch, J. (2015). Selenite-stress selected mutant strains of probiotic bacteria for Se source production. Journal of Trace Elements in Medicine and Biology 30, 96–101. https://doi.org/10.1016/j.jtemb.2014.11.003

Ringuet, M. T., Hunne, B., Lenz, M., Bravo, D. M. and Furness, J. B. (2021). Analysis of bioavailability and induction of glutathione peroxidase by dietary nanoelemental, organic and inorganic selenium. Nutrients. 13, 1073. https://doi.org/10.3390/nu13041073

Watanabe, L. M., Hashimoto, A. C., Torres, D. J., Berry, M. J. and Seale, L. A. 2020 Effects of selenium supplementation on diet-induced obesity in mice with a disruption of the selenocysteine lyase gene. Journal of Trace Elements in Medicine and Biology 62, 126596. https://doi.org/10.1016/j.jtemb.2020.126596.

Wu, Z., Bañuelos, G. S., Lin, Z. Q., Liu, Y., Yuan, L., Yin, X. and Li, M. (2015). Biofortification and phytoremediation of selenium in China. Frontiers in Plant Science 6, 136, https://doi.org/10.3389/fpls.2015.00136

Xu, C., Qiao, L., Guo, Y., Ma, L. and Cheng, Y. (2018). Preparation, characteristics and antioxidant activity of polysaccharides and proteins-capped selenium nanoparticles synthesized by Lactobacillus casei ATCC 393. Carbohydrate Polymers. 195, 576–585, https://doi.org/10.1016/j.carbpol.2018.04.110.

Zhang, B., Zhou, K., Zhang, J., Chen, Q., Liu, G., Shang, N., Qin, W., Li, P. and Lin, F. (2009). Accumulation and species distribution of selenium in Se-enriched bacterial cells of the Bifidobacterium animalis 01. Food Chemistry 115, 727–734. https://doi.org/10.1016/j.foodchem.2008.12.006

Zhang, J., Saad, R., Taylor, E. W. and Rayman, M. P. (2020a). Selenium and selenoproteins in viral infection with potential relevance to COVID-19. Redox Biology 37, 101715, https://doi.org/10.1016/j.redox.2020.101715.

Zhang, Y., Roh, Y. J., Han, S. J., Park, I., Lee, H. M., Ok, Y. S., Lee, B. C. and Lee, S. R. (2020b). Role of selenoproteins in redox regulation of signaling and the antioxidant system: A review. Antioxidants 9, 383. https://doi.org/10.3390/antiox9050383

Zhi-Qiang, J., Bo-Wen, Z. and Ping-Lan, L. (2009). Selenium tolerance and enrichment in Bifidobacterium animalis 01. Food Science 15, 104–110.

Zoidis, E., Seremelis, I., Kontopoulos, N. and Danezis, G. P. (2018). Selenium-dependent antioxidant enzymes: Actions and properties of selenoproteins. Antioxidants 7, 66. https://doi.org/10.3390/antiox7050066

Published
2022-10-14
How to Cite
Castañeda-Ovando, A., Pérez-Escalante, E., Rodríguez-Serrano, G., Martínez-Ramírez, X., Contreras-López, E., Jaimez-Ordaz, J., Añorve-Morga, J., Nieto-Velázquez, S., Ramírez-Godínez, J., & González Olivares, L. (2022). Selenium accumulation by Lactobacillus isolated from commercial fermented milk: minimum inhibitory concentration and kinetic growth changes. Revista Mexicana De Ingeniería Química, 21(3), Bio2824. https://doi.org/10.24275/rmiq/Bio2824
Section
Biotechnology

Most read articles by the same author(s)