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Interaction of lactic acid bacteria with metal ions: opportunities for improving food safety and quality

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Abstract

Certain species of lactic acid bacteria (LAB), as well as other microorganisms, can bind metal ions to their cells surface or transport and store them inside the cell. Due to this fact, over the past few years interactions of metal ions with LAB have been intensively investigated in order to develop the usage of these bacteria in new biotechnology processes in addition to their health and probiotic aspects. Preliminary studies in model aqueous solutions yielded LAB with high absorption potential for toxic and essential metal ions, which can be used for improving food safety and quality. This paper provides an overview of results obtained by LAB application in toxic metal ions removing from drinking water, food and human body, as well as production of functional foods and nutraceutics. The biosorption abilities of LAB towards metal ions are emphasized. The binding mechanisms, as well as the parameters influencing the passive and active uptake are analyzed.

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References

  • Alzate A, Cañas B, Pérez-Munguía S, Hernández-Mendoza H, Pérez-Conde C, Gutiérrez AM, Cámara C (2007) Evaluation of the inorganic selenium biotransformation in selenium-enriched yogurt by HPLC-ICP-MS. J Agric Food Chem 55(24):9776–9783

    Article  CAS  Google Scholar 

  • Alzate A, Fernández-Fernández A, Pérez-Conde C, Gutiérrez AM, Cámara C (2008) Comparison of biotransformation of inorganic selenium by Lactobacillus and Saccharomyces in lactic fermentation process of yogurt and kerfir. J Agric Food Chem 56:8728–8736

    Article  CAS  Google Scholar 

  • Andreoni V, Luischi MM, Cavalca L, Erba D, Ciappellano S (2000) Selenite tolerance and accumulation in the L. species. Ann Microbiol 50(1):77–88

    CAS  Google Scholar 

  • Araúz IL, Afton S, Wrobel K, Caruso JA, Corona JF, Wrobel K (2008) Study on the protective role of selenium against cadmium toxicity in LAB: an advanced application of ICP-MS. J Hazard Mater 153(3):1157–1164

    Article  Google Scholar 

  • Archibald FS, Fridovich I (1981) Manganese and defenses against oxygen toxicity in L. plantarum. J Bacteriol 145(1):442–451

    CAS  Google Scholar 

  • Battikh E, Safa A, Niccola MK, Aagha SI (2011) Effect of Cd and Lactobacillus levels on iron concentration in different organs and meat of broiler chicken. J Univ Chem Technol Metal 46(4):381–388

    CAS  Google Scholar 

  • Blackwell KJ, Singleton I, Tobin JM (1995) Metal cation uptake by yeast: a review. Appl Microbiol Biotechnol 43:579–584

    Article  CAS  Google Scholar 

  • Blanusa M, Varnai VM, Piasek M, Kostial K (2005) Chelators as antidotes of metal toxicity: therapeutic and experimental aspects. Curr Med Chem 12(23):2771–2794

    Article  CAS  Google Scholar 

  • Bolotin A, Wincker P, Mauger S, Jaillon O, Malarme K, Weissenbach J, Ehrlich SD, Sorokin A (2001) The complete genome sequence of the lactic acid bacterium L. lactis ssp. lactis IL1403. Genome Res 11:731–753

    Article  CAS  Google Scholar 

  • Bryszewska MA, Ambroziak W, Diowksz A, Baxter MJ, Langford NJ, Lewis DJ (2005) Changes in the chemical form of selenium observed during the manufacture of a selenium-enriched sourdough bread for use in a human nutrition study. Food Addit Contam 22(2):135–140

    Article  CAS  Google Scholar 

  • Bryszewska MA, Ambroziak W, Langford NJ, Baxter MJ, Colyer A, Lewis DJ (2007) The effect of consumption of selenium enriched rye/wheat sourdough bread on the body’s selenium status. Plant Foods Hum Nutr 62(3):121–126

    Article  CAS  Google Scholar 

  • Calomme MR, Van den Branden K, Vanden Berghe DA (1995a) Selenium and Lactobacillus species. J Appl Bacteriol 79:331–340

    Article  CAS  Google Scholar 

  • Calomme MR, Van den Branden K, Vanden Berghe DA (1995b) Seleno-Lactobacillus. An organic selenium source. Biol Trace Elem Res 47:379–384

    Article  CAS  Google Scholar 

  • Chen L, Pan D, Zhou J, Jiang YZ (2005) Protective effect of selenium-enriched lactobacillus on CCl4-induced liver injury in mice and it mechanisms. World J Gastroenterol 11(37):5795–5800

    CAS  Google Scholar 

  • Chojnacka K, Mikulewicz M, Cieplik J (2011) Biofortification off food with microelements. Am J Agric Biol Sci 6(4):544–548

    Article  CAS  Google Scholar 

  • Dalié DKD, Deschamps AM, Richard-Forget F (2010) Lactic acid bacteria—potential for control of mould growth and mycotoxins: a review. Food Control 21(4):370–380

    Article  Google Scholar 

  • Delcour J, Ferain T, Deghorain M, Palumbo E, Hols P (1999) The biosyntesis and functionality of the cell: wall of lactic acid bacteria. Universite Catolique de Louvain, Unite de Genetique, Croix du Sud 5, B-1348 Louvain-la-Neuve, Belgium

  • Diowksz A, Ambroziak W, Wladarezyk M (1999) Investigation of ability of selenium accumulation by lactic acid bacteria of Lactobacillus sp. and yeast S. cerevisiae. Pol J Food Nutr Sci 49(1):17–21

    Google Scholar 

  • Dobrzanski Z, Jamroz D (2003) Bioavailability of selenium and zinc supplied to the feed for laying hens in organic and inorganic form. EJPAU 6:1–8

    Google Scholar 

  • Duhutrel P, Bordat C, Wu TD, Zagorec M, Guerquin-Kern JL, Champomier-Vergès MC (2012) Iron sources used by the nonpathogenic lactic acid bacterium L. sakei as revealed by electron energy loss spectroscopy and secondary-ion mass spectrometry. Appl Environ Microbiol 78(11):560–565

    Google Scholar 

  • El-Nezami H, Kankaanpaa P, Salminen S, Ahokas J (1998) Physicochemical alterations enhance the ability of dairy strains of lactic acid bacteria to remove aflatoxin from contaminated media. J Food Prot 61(4):466–468

    CAS  Google Scholar 

  • Frece J, Kos B, Beganovic J, Vukovic S, Suskovic J (2005) In vivo testing of functional properties of three selected probiotic strains. World J Microbiol Biotechnol 21:1401–1408

    Article  Google Scholar 

  • Gerbino E, Mobili P, Tymczyszyn E, Fausto R, Gomez-Zavaglia A (2011) FTIR spectroscopy structural analysis of the interaction between L. kefir S-layers and metal ions. J Mol Struct 987(1–3):186–192

    Article  CAS  Google Scholar 

  • Gulan-Zetić V, Stehlik-Tomas V, Grba S, Lutilsky L, Kozlek D (2001) Chromium uptake by S. cerevisiae and isolation of glucose tolerance factor from yeast biomass. J Biosci 26(2):217–223

    Article  Google Scholar 

  • Halttunen T, Kankaanpaa P, Tahvonen R, Salminen S, Ouwehand AC (2003) Cadmium removal by specific lactic acid bacteria. Biosci Microflora 22(3):93–97

    CAS  Google Scholar 

  • Halttunen T, Salminen S, Tahvonen R (2007a) Rapid removal of lead and cadmium from water by specific lactic acid bacteria. Int J Food Microbiol 114:30–35

    Article  CAS  Google Scholar 

  • Halttunen T, Finell M, Salminen S (2007b) Arsenic removal by native and chemically modified lactic acid bacteria. Int J Food Microbiol 120(1–2):173–178

    Article  CAS  Google Scholar 

  • Halttunen T, Salminen S, Meriluoto J, Tahvonen R (2008a) Reversible surface binding of cadmium and lead by lactic acid and bifidobacteria. Int J Food Microbiol 125(2):170–175

    Article  Google Scholar 

  • Halttunen T, Collado MC, El-Nezami H, Meriluoto J, Salminen S (2008b) Combining strains of lactic acid bacteria may reduce their toxin and heavy metal removal efficiency from aqueous solution. Lett Appl Microbiol 46:160–165

    Article  CAS  Google Scholar 

  • Heyland DK, Dhaliwal R, Suchner U, Berger MM (2005) Antioxidant nutrients: a systematic review of trace elements and vitamins in the critically ill patient. Intensive Care Med 31:327–337

    Article  Google Scholar 

  • Ibrahim F, Halttunen T, Tahvonen R, Salminen S (2006) Probiotic bacteria as potential detoxification tools: assessing their heavy metal binding isotherms. Can J Microbiol 52:877–885

    Article  CAS  Google Scholar 

  • Imbert M, Blondeau R (1998) On the iron requirement of Lactobacilli grown in chemically defined medium. Curr Microbiol 37:64–66

    Article  CAS  Google Scholar 

  • Lamberti C, Mangiapane E, Pessione A, Mazzoli R, Giunta C, Pessione E (2011) Proteomic characterization of a selenium-metabolizing probiotic L. reuteri Lb2 BM for nutraceutical applications. Proteomics 11(11):2212–2221

    Article  CAS  Google Scholar 

  • Leroy F, De Vuyst L (2004) Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Tech 15(2):67–78

    Article  CAS  Google Scholar 

  • Lin Z, Zhou C, Wu J, Zhou J, Wang L (2005) A further insight into the mechanism of Ag+ biosorption by Lactobacillus sp. Strain A09. Spectrochim Acta, Part A 61:1195–1200

    Article  Google Scholar 

  • Liu W, Deng Z, Xu E, Li M (2006) Bioconcentrating trace elements of selenium, chromium and zinc by L. bulgaricus. Food Sci Technol 2:135–137

    CAS  Google Scholar 

  • Llull D, Son O, Blanié S, Briffotaux J, Morello E, Rogniaux H, Danot O, Poquet I (2011) Lactococcus lactis ZitR is a zinc-responsive repressor active in the presence of low, nontoxic zinc concentrations in vivo. J Bacteriol 193(8):1919–1929

    Article  CAS  Google Scholar 

  • Mazo VK, Gmoshinski IV, Zorin SN (2007) New food sources of essential trace elements produced by biotechnology facilities. Biotechnol J 2(10):1297–1305

    Article  CAS  Google Scholar 

  • Mrvcic J, Stanzer D, Stehlik-Tomas V, Skevin D, Grba S (2007) Optimization of bioprocess for production of copper-enriched biomass of industrially important microorganism S. cerevisiae. J Biosci Bioeng 103(4):331–337

    Article  CAS  Google Scholar 

  • Mrvcic J, Stehlik-Tomas V, Grba S (2008) Incorporation of copper ions by yeast K. marxianus during cultivation on whey. Acta Aliment 37(1):133–139

    Article  CAS  Google Scholar 

  • Mrvčić J, Prebeg T, Barišić L, Stanzer D, Bačun-Družina V, Stehlik-Tomas V (2009a) Zinc binding by lactic acid bacteria. Food Technol Biotechnol 47(4):381–388

    Google Scholar 

  • Mrvčić J, Stanzer D, Bačun-Družina V, Stehlik-Tomas V (2009b) Copper binding by lactic acid bacteria (LAB). Biosci Microflora 28(1):1–6

    Google Scholar 

  • Mrvčić J, Šolić E, Butorac A, Stanzer D, Bačun-Družina V, Stehlik-Tomas V (2011) The effect of metal ions supplementation on growth and binding capacity of lactic acid bacteria/7th international congress of food technologists, biotecnologists and nutritionist/Medić, H. (ur.). Zagreb: Baris, Zaprešić, 67–67

  • Mudgal V, Madaan N, Anurag Mudgal RB, Mishra SS (2010) Effect of toxic metals on human health. Open Nutraceuticals J 3:94–99

    Article  CAS  Google Scholar 

  • Mudronova D, Nemecova R, Gancarčikova S, Bomba A, Gyoryova K (2004) Influence of Zn2+ and Lactobacillus plantarum CCM 7102 on the composition microflora in laboratory mice. University of veterinary medicine, Komenskeho 73, 041 81 Košice, Slovak Republic

  • Naumann D, Helm D, Labischinski H, Giesbrecht P (1991) The characterization of microorganism by Fourier-transform infrared spectroscopy. In: Nelson WH (ed) Modern techniques for rapid microbiological analysis. VCH, New York, pp 43–96

    Google Scholar 

  • Nielsen MM, Damstrup ML, Thomsen A, Kjærsg S, Hansen R (2007) Phytase activity and degradation of phytic acid during rye bread making. Eur Food Res Technol 225:173–181

    Article  CAS  Google Scholar 

  • Pandey A, Bringel F, Meyer JM (1994) Iron requirement and search for siderophores in lactic acid bacteria. Appl Microbiol Biotechnol 40:735–739

    Article  CAS  Google Scholar 

  • Papp LV, Lu J, Holmgren A, Khanna KK (2007) From selenium to selenoproteins: synthesis, identity, and their role in human health. Antioxid Redox Signal 9(7):776–806

    Article  Google Scholar 

  • Peñas E, Martinez-Villaluenga C, Frias J, Sánchez-Martínez MJ, Pérez-Corona MT, Madrid Y, Cámara C, Vidal-Valverde C (2012) Se improves indole glucosinolate hydrolysis products content, Se-methylselenocysteine content, antioxidant capacity and potential anti-inflammatory properties of sauerkraut. Food Chem 132(2):907–914

    Article  Google Scholar 

  • Pérez-Corona MT, Sánchez-Martínez M, Valderrama MJ, Rodríguez ME, Cámara C, Madrid Y (2011) Se biotransformation by S. cerevisiae and S. bayanus during white wine manufacture: lab-scale experiments. Food Chem 124:1050–1055

    Article  Google Scholar 

  • Rayman MP (2004) The use of high-selenium yeast to raise selenium status: how does it measure up? Br J Nutr 92:557–573

    Article  CAS  Google Scholar 

  • Rodriguez LM, Alatossava T (2008) Effects of copper supplement on growth and viability of strains used as starters and adjunct cultures for Emmental cheese manufacture. J Appl Microbiol 105:1098–1106

    Article  CAS  Google Scholar 

  • Ruas-Madiedo P, Hugenholtz J, Zoon P (2002) An overview of the functionality of exopolysaccharides produced by lactic acid bacteria. Int Dairy J 12:163–171

    Article  CAS  Google Scholar 

  • Salim AB, Badawy IH, Kassem SS (2011) Effect of lactic acid bacteria against heavy metals toxicity in rats. J Am Sci 7(4):264–274

    Google Scholar 

  • Schut S, Zauner S, Hampel G, König H, Claus H (2011) Biosorption of copper by wine-relevant lactobacilli. Int J Food Microbiol 145(1):126–131

    Article  CAS  Google Scholar 

  • Simić D, Budić I (2003) Trace elements. Acta Fac Med Naiss 20(4):189–202

    Google Scholar 

  • Solioz M, Abicht HK, Mermod M, Mancini S (2010) Response of Gram-positive bacteria to copper stress. J Biol Inorg Chem 15:3–14

    Article  CAS  Google Scholar 

  • Stefanidou M, Maravelias C, Dona A, Spilliopoulou C (2006) Zinc: a multipurpose trace element. Arch Toxicol 80:1–9

    Article  CAS  Google Scholar 

  • Stein AJ, Meenakshi JV, Qaim M, Nestel P, Sachdev HPS (2008) Potential impacts of iron biofortification in India. Soc Sci Med 66:1797–1808

    Article  Google Scholar 

  • Suhajda A, Hegoczki J, Janzso B, Pais I, Vereczkey G (2000) Preparation of selenium yeasts I. Preparation of selenium-enriched S. cerevisiae. J Trace Elem Med Biol 14:43–47

    Article  CAS  Google Scholar 

  • Urban PL, Kuthan RT (2004) Application of probiotics in the xenobiotic detoxification therapy. Nukleonika 49:43–45

    Google Scholar 

  • Vijayaraghavan K, Yun YS (2008) Bacterial biosorbents and biosorption. Biotechnol Adv 26(3):266–291

    Article  CAS  Google Scholar 

  • Vinodhini R, Narayanan M (2008) Bioaccumulation of heavy metals in organs of fresh water fish Cyprinus carpio (common carp). Int J Environ Sci Tech 5(2):179–182

    CAS  Google Scholar 

  • Volesky B, May-Phillips HA (1995) Biosorption of heavy metals by S. cerevisae. Appl Microbiol Biotechnol 42:797–806

    Article  CAS  Google Scholar 

  • Wang J, Chen C (2009) Biosorbent of heavy metals removal and their future. Biotechnol Adv 27:195–226

    Article  Google Scholar 

  • Xia KS, Chen L, Liang JQ (2007) Enriched selenium and its effects on growth and biochemical composition in L. bulgaricus. J Agric Food Chem 55:2413–2417

    Article  CAS  Google Scholar 

  • Yang J, Huang K, Qin S, Wu X, Zhao Z, Chen F (2009) Antibacterial action of selenium-enriched probiotics against pathogenic E. coli. Dig Dis Sci 54:246–254

    Article  CAS  Google Scholar 

  • Yilmaz M, Tay T, Kivanc M, Turk H (2010) Removal of copper ions from aqueous solution by lactic acid bacterium. Braz J Chem Eng 27(2):309–314

    Article  CAS  Google Scholar 

  • Zhang B, Zhou K, Zhang J, Chen Q, Liu G, Shang N, Qin W, Li P, Lin F (2009) Accumulation and species distribution of selenium in Se-enriched bacterial cells of the B. animalis 01. Food Chem 115(2):727–734

    Article  CAS  Google Scholar 

  • Zhao FJ, McGrath SP (2009) Biofortification and phytoremediation. Curr Opin Plant Biol 12:373–380

    Article  CAS  Google Scholar 

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Acknowledgments

The authors are grateful for financial support from The Ministry of Science and Technology of Republic Croatia.

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  1. Faculty of Food Technology and Biotechnology, Laboratory for Fermentation and Yeast Technology, Pierottijeva 6, 10000, Zagreb, Croatia

    Jasna Mrvčić, Damir Stanzer, Ema Šolić & Vesna Stehlik-Tomas

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  1. Jasna Mrvčić
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  2. Damir Stanzer
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Correspondence to Jasna Mrvčić.

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

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  • DOI: https://doi.org/10.1007/s11274-012-1094-2

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