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Removal of cadmium by Lactobacillus kefir as a protective tool against toxicity

Published online by Cambridge University Press:  24 June 2014

Esteban Gerbino ,
Paula Carasi ,
E. Elizabeth Tymczyszyn  and
Andrea Gómez-Zavaglia
Esteban Gerbino
Affiliation:
Center for Research and Development in Food Cryotechnology, CCT-CONICET La Plata, RA-1900, Argentina
Paula Carasi
Affiliation:
Laboratorio de Microbiología, Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, Argentina
E. Elizabeth Tymczyszyn
Affiliation:
Center for Research and Development in Food Cryotechnology, CCT-CONICET La Plata, RA-1900, Argentina
Andrea Gómez-Zavaglia*
Affiliation:
Center for Research and Development in Food Cryotechnology, CCT-CONICET La Plata, RA-1900, Argentina
*
*For correspondence; e-mail: angoza@qui.uc.pt
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Abstract

The aim of this work was to evaluate the capacity of Lactobacillus kefir strains to remove cadmium cations and protect eukaryotic cells from cadmium toxicity. Lb. kefir CIDCA 8348 and JCM 5818 were grown in a 1/2 dilution of MRS broth supplemented with Cd(NO3)2 ranging 0 to 1 mM. Growth kinetics were followed during 76 h at 30 °C by registering optical density at 600 nm every 4–10 h. The accumulated concentration of cadmium was determined on cultures in the stationary phase by atomic absorption. The viability of a human hepatoma cell line (HepG2) upon exposure to (a) free cadmium and (b) cadmium previously incubated with Lb. kefir strains was evaluated by determining the mitochondrial dehydrogenase activity. Lb. kefir strains were able to grow and tolerate concentrations of cadmium cations up to 1 mM. The addition of cadmium to the culture medium increased the lag time in all the concentrations used. However, a decrease of the total biomass (maximum Absorbance) was observed only at concentrations above 0·0012 and 0·0011 mM for strains CIDCA 8348 and JCM 5818, respectively. Shorter and rounder lactobacilli were observed in both strains upon microscopic observations. Moreover, dark precipitates compatible with intracellular precipitation of cadmium were observed in the cytoplasm of both strains. The ability of Lb. kefir to protect eukaryotic cells cultures from cadmium toxicity was analysed using HepG2 cells lines. Concentrations of cadmium greater than 3×10−3 mM strongly decreased the viability of HepG2 cells. However, when the eukaryotic cells were exposed to cadmium pre-incubated 1 h with Lb. kefir the toxicity of cadmium was considerably lower, Lb. kefir JCM 5818 being more efficient. The high tolerance and binding capacity of Lb. kefir strains to cadmium concentrations largely exceeding the tolerated weekly intake (TWI) of cadmium for food (2.5 μg per kg of body weight) and water (3 μg/l) addressed to human consumption, is an important added value when thinking in health-related applications.

Keywords

CadmiumLb. kefirprobioticsbioaccumulationHepG2 cells
Type
Research Article
Information
Journal of Dairy Research , Volume 81 , Issue 3 , August 2014 , pp. 280 - 287
Copyright
Copyright © Proprietors of Journal of Dairy Research 2014 

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References

Adarsh, VK, Mishra, M, Chowdhury, S, Sudarshan, M, Thakur, AR & Chaudhuri, SR 2007 Studies on metal microbe interaction of three bacterial isolates from east Calcutta wetland. OnLine Journal Biological Sciences 7 80–88Google Scholar
Agency for Toxic Substances and Disease Registry (ATSDR) 2008 Toxicological profile for Cadmium (Draft for Public Comment). Atlanta, GA: U.S. Department of Health and Human Services, Public Health Service. http://www.atsdr.cdc.gov. Agency for Toxic Substances and Disease Registry. Toxicological Profile for CadmiumGoogle Scholar
Bhakta, JN, Ohnishi, K, Munekage, Y, Iwasaki, K & Wei, MQ 2012 Characterization of lactic acid bacteria-based probiotics as potential heavy metal sorbents. Journal of Applied Microbiology 112 1193–1206CrossRefGoogle ScholarPubMed
Battikh, E, Safa, A, Niccola, MK & Aagha, SI 2011 Effect of cadmium and Lactobacillus levels on iron concentration in different organs and meat of broiler chicken. Journal of the University of Chemical Technology and Metallurgy 46 381–388Google Scholar
Carballo, R, Castiñeiras, A, Domínguez-Martín, A, García-Santos, I & Niclós-Gutiérrez, J 2012 Solid state structures of cadmium complexes with relevance for biological systems. In Cadmium: From Toxicity to Essentiality. Series: Metal ions in Life Sciences, Chapter 7, pp. 145–189 (Eds Sigel, A, Sigel, H & Sigel, RKO). Springer ebooks.Google Scholar
Cervantes, C, Espino-Saldaña, AE, Acevedo-Aguilar, F, León-Rodríguez, IL, Rivera-Cano, ME, Avila-Rodríguez, M, Wróbel-Kaczmarczyk, K, Wróbel-Zasada, K, Gutiérrez-Corona, JF, Rodríguez-Zavala, JS & Moreno-Sánchez, R 2006 Interacciones microbianas con metales pesados. Revista Latinoamericana Microbiologia 48 203–210Google Scholar
Crichton, RR 2007 Metals in medicine and the environment. Cadmium. In Biological Inorganic Chemistry. An Introduction, Chapter 20, pp. 346–350. Oxford: ElsevierGoogle Scholar
Del Piano, M, Carmagnola, S, Anderloni, A, Andorno, S, Ballarè, M, Balzarini, M, Montino, F, Orsello, M, Pagliarulo, M, Sartori, M, Tari, R, Sforza, F & Capurso, L 2010 The use of probiotics in healthy volunteers with evacuation disorders and hard stools: a double-blind, randomized, placebo-controlled study. Journal of Clinical Gastroenterology 44 S30–34CrossRefGoogle ScholarPubMed
De Man, JO, Rogosa, M & Sharpe, ME 1960 A medium for the cultivation of lactobacilli. Journal of Applied Bacteriology 23 130–135Google Scholar
European Food Safety Authority (EFSA) 2012 Cadmium dietary exposure in the European population. EFSA Journal 10 2551. [37 pages; doi:10.2903/j.efsa.2012.2551. Available: www.efsa.europa.eu/efsajournal [Accessed 5th October 2013]Google Scholar
Fotakis, G & Timbrell, JA 2006 In vitro cytotoxicity assays: comparison of LDH, neutral red, MTT and protein assay in hepatoma cell lines following exposure to cadmium chloride. Toxicology Letters 160 171–177Google Scholar
García, H, Senior, A, El Zauahre, M, Morán, H, Acosta, Y & Femández, N 2006 Análisis comparativo de dos técnicas de digestión para la determinación de metales pesados en Iodos residuales. Multiciencias 6 234–243Google Scholar
Garrote, GL, Abraham, AG & De Antoni, GL 2001 Chemical and microbiological characterisation of kefir grains. Journal of Dairy Research 68 639–652Google Scholar
Gerbino, E, Mobili, P, Tymczyszyn, EE, Fausto, R & Gómez-Zavaglia, A 2011 FTIR spectroscopy structural analysis of the interaction between Lactobacillus kefir S-layers and metal ions. Journal of Molecular Structure 987 186–192Google Scholar
Gerbino, E, Mobili, P, Tymczyszyn, EE, Frausto Reyes, C, Araujo-Andrade, C & Gómez-Zavaglia, A 2012 Use of Raman spectroscopy and chemometrics for the quantification of metal ions attached to Lactobacillus kefir. Journal Applied Microbiology 112 363–371Google Scholar
Golowczyc, MA, Mobili, P, Garrote, GL, Abraham, AG & De Antoni, GL 2007 Protective action of Lactobacillus kefir carrying S-layer protein against Salmonella enterica serovar Enteritidis. International Journal of Food Microbiology 118 264–273CrossRefGoogle ScholarPubMed
Halttunen, T, Salminen, S & Tahvonen, R 2007 Rapid removal of lead and cadmium from water by specific lactic acid bacteria. International Journal Food Microbiology 114 30–35Google Scholar
Hynninen, A 2010 Zinc, cadmium and lead resistance mechanisms in bacteria and their contribution to biosensing. PhD Thesis. Finland: Department of Food and Environmental Sciences, Faculty of Agriculture and Forestry, University of HelsinkiGoogle Scholar
Monachese, M 2012 Sequestration of lead, cadmium and arsenic by Lactobacillus species and detoxification potential. Master of Science Thesis. London, Ontario, Canada: University of Western OntarioGoogle Scholar
Mosmann, T 1983 Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunological Methods 65 55–63Google Scholar
Mrvcic, J, Stanzer, D, Solic, E & Stehlik-Tomas, V 2012 Interaction of lactic acid bacteria with metal ions: opportunities for improving food safety and quality. World Journal of Microbioly and Biotechnology 28 2771–2782Google Scholar
Panwichian, S, Kantachote, D, Wittayaweerasak, B & Mallavarapu, M 2011 Removal of heavy metals by exopolymeric substances produced by resistant purple nonsulfur bacteria isolated from contaminated shrimp ponds. Electronic Journal of Biotechnology 14 4Google Scholar
Prasad, K & Jha, AK 2010 Biosynthesis of CdS nanoparticles: an improved green and rapid procedure. Journal of Colloid Interface Science 342 68–72CrossRefGoogle ScholarPubMed
Rial, D, Vázquez, JA & Murado, MA 2011 Effects of three heavy metals on the bacteria growth kinetics: a bivariate model for toxicological assessment. Applied Microbiology and Biotechnology 90 1095–1109Google Scholar
Salim, AB, Badawy, IH & Kassem, SS 2011 Effect of lactic acid bacteria against heavy metals toxicity in rats. Journal of American Science 7 264–274Google Scholar
Satarug, S, Garrett, SH, Sens, MA & Sens, DA 2010 Cadmium, environmental exposure, and health outcomes. Environmental and Health Perspectives 118 182–190CrossRefGoogle ScholarPubMed
Urban, PL & Kuthan, RT 2004 Application of probiotics in the xenobiotic detoxification therapy. Nukleonika 49 43–45Google Scholar
World Health Organization (WHO) 1989 Evaluation of Certain Food Additives and Contaminants. Thirty-third Report of the Joint FAO/WHO Expert Committee on Food Additives. WHO Technical Report Series 776. Available: http://www.who.int/ipcs/publications/jecfa/reports/en/index.html [accessed 2nd October 2013]Google Scholar
World Health Organization (WHO) 2006 Guidelines for Drinking-water Quality. Vol. 1, Recommendaciones–3rd ed. Available in: http://www.who.int/water_sanitation_health/dwq/gdwq3rev/en/index.htmGoogle Scholar
Zhai, Q, Wang, G, Zhao, J, Liu, X, Tian, F, Zhang, H & Chen, W 2013 Protective effects of Lactobacillus plantarum CCFM8610 against acute cadmium toxicity in mice. Applied and Environmental Microbiology 79 1508–1515CrossRefGoogle ScholarPubMed
Zheng, Y, Lu, Y, Wang, J, Yang, L, Pan, C & Huang, Y 2013 Probiotic properties of Lactobacillus strains isolated from Tibetan kefir grains. PLoS ONE 8 e69868Google Scholar