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Effect of selenium supplements on the antioxidant activity and nitrite degradation of lactic acid bacteria

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Abstract

Selenium (Se) is one of the essential trace elements in the human body, and Se-enriched lactic acid bacteria (LAB) can improve the biological utilization value of inorganic Se. The aim of this study was to isolate Se-enriched LAB and study their effects on antioxidant activity and nitrite degradation. The Se-enriched LAB L.P2, which was nitrite-tolerant and could grow in 30 µg/mL sodium selenite (Na2SeO3) medium, was isolated from the traditional fermented Chinese sauerkraut. L.P2 belonged to Lactobacillus plantarum according to the 16S rDNA analysis. The biomass and lactic acid production of L.P2 reached to a maximum (9.52 log CFU/mL and 16.99 mg/mL) when 2.0 µg/mL Na2SeO3 was supplemented in the medium. Additionally, the nitrite degradation rate reached 85.76% when the initial concentration of Na2SeO3 was 2.0 µg/mL. The Se-enriched LAB enhanced the scavenging capacity of hydroxyl radical and superoxide free radical of L.P2 and improved the lipid peroxidation and ion-chelating abilities. Moreover, the activities of superoxide dismutase (SOD) and glutathione peroxidase (GSH-Px) in Se 4 group (4.0 µg/mL Na2SeO3 was added) reached 48.49 and 50.35 U/mg, respectively. Thus, Se 4 concentration was significantly higher than that of Se 0 group (with no Se added). In particular, SOD and GSH-Px enzymes correlated with nitrite degradation (P < 0.01). Collectively, our results indicate that Se supplementation can enhance the antioxidant capacity of LAB, contribute to its nitrite degradation, and thus may have potential applications in functional foods.

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References

  • Abdulah R, Miyazaki K, Nakazawa M, Koyama H (2005) Chemical forms of selenium for cancer prevention. J Trace Elem Med Bio 19(2–3):141

    Article  CAS  Google Scholar 

  • Alzate A, Cañas B, Pérezmunguía S, Hernándezmendoza H, Pérezconde 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  PubMed  Google Scholar 

  • Alzate A, Ferna´ndez-Ferna´ndez A, Perez-Conde M, Gutie´rrez A, Ca´mara C (2008) Comparison of biotransformation of inorganic selenium by Lactobacillus and Saccharomyces in lactic fermentation process of yogurt and kefir. J Agric Food Chem 56(18):8728–8736

    Article  CAS  PubMed  Google Scholar 

  • Alzate A, Pérezconde MC, Gutiérrez AM, Cámara C (2010) Selenium-enriched fermented milk: a suitable dairy product to improve selenium intake in humans. Int Dairy J 20(11):761–769

    Article  CAS  Google Scholar 

  • Ammor MS, Mayo B (2007) Selection criteria for lactic acid bacteria to be used as functional starter cultures in dry sausage production: an update. Meat Sci 76(1):138–146

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Behne D, Alber D, Kyriakopoulos A (2010) Long-term selenium supplementation of humans: selenium status and relationships between selenium concentrations in skeletal muscle and indicator materials. J Trace Elem Med Bio 24(2):99

    Article  CAS  Google Scholar 

  • Bozkurt H, Bayram M (2006) Colour and textural attributes of sucuk during ripening. Meat Sci 73(2):344–350

    Article  PubMed  Google Scholar 

  • Calomme M, Hu J, Van DBK, Vanden Berghe DA (1995) Seleno-lactobacillus. An organic selenium source. Biol Trace Elem Res 47(1–3):379

    Article  CAS  PubMed  Google Scholar 

  • Chan TYK (2011) Vegetable-borne nitrate and nitrite and the risk of methaemoglobinaemia. Toxicol Lett 200(1–2):107–108

    Article  CAS  PubMed  Google Scholar 

  • Chang MW Edirisinghe M, Stride E (2013) Ultrasound mediated release from stimuli-responsive core–shell capsules. J Mater Chem B 1(32):3962–3971

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Bai Y, Li D, Wang C, Xu N, Hu Y (2016) Screening and characterization of ethanol-tolerant and thermotolerant acetic acid bacteria from Chinese vinegar Pei. World J Microb Biot 32(1):14

    Article  CAS  Google Scholar 

  • Con AH, Gokalp HY (2000) Production of bacteriocin-like metabolites by lactic acid cultures isolated from sucuk samples. Meat Sci 55(1):89–96

    Article  CAS  PubMed  Google Scholar 

  • Cui Y, Qu X, Li H, He S, Liang H, Zhang H, Ma Y (2012) Isolation of halophilic lactic acid bacteria from traditional Chinese fermented soybean paste and assessment of the isolates for industrial potential. Eur Food Res Technol 234(5):797–806

    Article  CAS  Google Scholar 

  • Dellavalle CT, Xiao Q, Yang G, Shu XO, Aschebrookkilfoy B, Zheng W, Chow WH (2014) Dietary nitrate and nitrite intake and risk of colorectal cancer in the Shanghai Women’s Health Study. Int J Gynecol Cancer 134(12):2917–2926

    Article  CAS  Google Scholar 

  • Deng Y, Man C, Fan Y, Wang Z, Li L, Ren H, Jiang Y (2015) Preparation of elemental selenium-enriched fermented milk by newly isolated Lactobacillus brevis from kefir grains. Int Dairy J 44:31–36

    Article  CAS  Google Scholar 

  • Di CR, Surico RF, Minervini G, Rizzello CG, Lovino R, Servili M (2011) Exploitation of sweet cherry (prunus avium l.) puree added of stem infusion through fermentation by selected autochthonous lactic acid bacteria. Food Microbiol 28(5):900–909

    Article  CAS  Google Scholar 

  • Eszenyi P, Sztrik A, Babka B, Prokisch J (2011) Elemental, nano-sized (100–500 nm) selenium production by probiotic lactic acid bacteria. Inter J Biosci Biochem Bioinform 1(2):148–152

    Google Scholar 

  • Fairweathertait SJ, Collings R, Hurst R (2010) Selenium bioavailability: current knowledge and future research requirements. Am J Clin Nutr 2010, 91(5):1484

    Article  CAS  Google Scholar 

  • Fang F, Feng T, Du G, Chen J (2016) Evaluation of the impact on food safety of a Lactobacillus coryniformis strain from pickled vegetables with degradation activity against nitrite and other undesirable compounds. Food Addit Contam 33(4):623–630

    CAS  Google Scholar 

  • Farahnak A, Golestani A, Eshraghian MR (2013) Activity of superoxide dismutase (SOD) enzyme in the excretory-secretory products of Fasciola hepatica and F. gigantica parasites. Iran J Parasitol 8(1):167

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jr Fridovich BW I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161(2):559–566

    Article  PubMed  Google Scholar 

  • González A, Ngel Mas A (2011) Differentiation of acetic acid bacteria based on sequence analysis of 16S-23S rRNA gene internal transcribed spacer sequences. Int J Food Microbiol 147(3):217–222

    Article  PubMed  CAS  Google Scholar 

  • Guo Y, Pan D, Li H, Sun Y, Zeng X, Yan B (2015) Antioxidant and immunomodulatory activity of selenium exopolysaccharide produced by lactococcus lactis subsp. lactis. Food Chem 26(2):248–259

    Google Scholar 

  • Halliwell B, Gutteridge JM (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219(1):1–14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halliwell B, Murcia MA, Chirico S, Aruoma OI (1995) Free radicals and antioxidants in food and in vivo: what they do and how they work. Crit Rev Food Sci Nutr 35(1–2):7–20

    Article  CAS  PubMed  Google Scholar 

  • Hansen SA (1976) Thin-layer chromatographic method for the identification of organic acids. J Chromatogr A 124(1):123–126

    Article  CAS  Google Scholar 

  • Hatfield DL, Tsuji PA, Carlson BA, Gladyshev VN (2014) Selenium and selenocysteine: roles in cancer, health and development. Trends Biochem Sci 39(3):112–120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He ZS, Cao ZH, Jian D (2004) Photometric determination of hydroxyl free radical in Fenton system by toluidine blue. Chin J Health Lab Technol 6:236–237

    Google Scholar 

  • Hugas M, Monfort JM (1997) Bacterial starter cultures for meat fermentation. Food Chem 59(4):547–554

    Article  CAS  Google Scholar 

  • Hurst R, Hooper L, Norat T, Lau R, Aune D, Greenwood DC, Sterne JA (2012) Selenium and prostate cancer: systematic review and meta-analysis. Am J Clin Nutr 96(1):1111–1122

    Article  CAS  Google Scholar 

  • Jagannath A, Raju PS, Bawa AS (2012) A two-step controlled lactic fermentation of cabbage for improved chemical and microbiological qualities. J Food Quality 35(1):13–20

    Article  CAS  Google Scholar 

  • Keshari V, Adeeb B, Simmons AE, Simmons TW, Diep CQ (2016) Zebrafish as a model to assess the teratogenic potential of nitrite. J Vis Exp 108(108):53615

    Google Scholar 

  • Kiełczykowska M, Kocot J, Paździor M, Musik I (2018) Selenium-a fascinating antioxidant of protective properties. Adv Clin Exp Med 27(2):245–255

    Article  PubMed  Google Scholar 

  • Korhola M, Vainio A, Edelmann K (1986) Selenium yeast. Ann Clin Res 18(1):65

    CAS  PubMed  Google Scholar 

  • Kullisaar T, Zilmer M, Mikelsaar M, Vihalemm T, Annuk H, Kairane C, Kilk A (2002) Two antioxidative lactobacilli strains as promising probiotics. Int J Food Microbiol 72(3):215–224

    Article  CAS  PubMed  Google Scholar 

  • Li S, Zhao Y, Zhang L, Zhang X, Huang L, Li D, Wang Q (2012) Antioxidant activity of Lactobacillus plantarum strains isolated from traditional Chinese fermented foods. Food Chem 135(3):1914–1919

    Article  CAS  PubMed  Google Scholar 

  • Lin MY, Yen CL (1999) Antioxidative ability of lactic acid bacteria. J Agric Food Chem 47(4):1460–1466

    Article  CAS  PubMed  Google Scholar 

  • Lin Y, Totsuka Y, He Y (2013) Epidemiology of esophageal cancer in Japan and China. J Epidemiol 23(4):233

    Article  PubMed  Google Scholar 

  • Liu DM, Wang P, Zhang XY, Xu XL, Wu H, Li L (2014) Characterization of nitrite degradation by Lactobacillus casei subsp. rhamnosus LCR 6013. PLoS ONE, 9(4), e93308

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lopes G, Ávila FW, Guilherme LRG (2017) Selenium behavior in the soil environment and its implication for human health. Ciênc Agrotecnol 41(6):605–615

    Article  CAS  Google Scholar 

  • Lucy JA (1972) Functional and structural aspects of biological membranes: a suggested structural role for vitamin E in the control of membrane permeability and stability. Ann NY Acad Sci 203(1):4–11

    Article  CAS  PubMed  Google Scholar 

  • Manda K, Bhatia AL (2003) Prophylactic action of melatonin against cyclophosphamide-induced oxidative stress in mice. Cell Biol Toxicol 19(6):367

    Article  CAS  PubMed  Google Scholar 

  • Mashmouli B (2013) Selenium as an effective element for lung cancer prevention and treatment. KUMS J 16(7):693–694

    Google Scholar 

  • Oh CK, Oh MC, Kim SH (2004) The depletion of sodium nitrite by lactic acid bacteria isolated from kimchi. J Med Food 7(1):38–44

    Article  CAS  PubMed  Google Scholar 

  • Oldfield EH, Loomba JJ, Monteith SJ, Crowley RW, Medel R, Gress DR (2013) Safety and pharmacokinetics of sodium nitrite in patients with subarachnoid hemorrhage: a phase iia study. J Neurosurg 119(3):634–641

    Article  CAS  PubMed  Google Scholar 

  • Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70(1):158–169

    CAS  PubMed  Google Scholar 

  • Paik HD, Lee JY (2014) Investigation of reduction and tolerance capability of lactic acid bacteria isolated from kimchi against nitrate and nitrite in fermented sausage condition. Meat Sci 97(4):609–614

    Article  CAS  PubMed  Google Scholar 

  • Palomo M, Gutiérrez AM, Pérez-Conde MC, Cámara C, Madrid Y (2014) Se metallomics during lactic fermentation of Se-enriched yogurt. Food Chem 164:371–379

    Article  CAS  Google Scholar 

  • Peñas E, Martinezvillaluenga C, Frias J, Sánchezmartínez MJ, Pérezcorona MT, Madrid Y, Vidalvalverde 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  CAS  Google Scholar 

  • Pescuma M, Gomez-Gomez B, Perez-Corona T, Font G, Madrid Y, Mozzi F (2017) Food prospects of selenium enriched-Lactobacillus acidophilus CRL 636 and Lactobacillus reuteri CRL 1101. J Funct Foods 35:466–473

    Article  CAS  Google Scholar 

  • Pilarczyk B, Szewczuk M, Pilarczyk R, Tomza-Marciniak A, Marciniak A, Dobrzanski Z, Bakowska M (2016) Effect of supplementing selenized yeast to ewes from an organic farm on serum Se concentration in lambs. J Elementol 21(4):1093–1101

    Google Scholar 

  • Pophaly SD, Poonam Singh P, Kumar H, Tomar SK, Singh R (2014) Selenium enrichment of lactic acid bacteria and bifidobacteria: a functional food perspective. Trends Food Sci Technol 39(2):135–145

    Article  CAS  Google Scholar 

  • Ren Z, Zhao Z, Wang Y, Huang K (2011) Preparation of selenium/zinc-enriched probiotics and their effect on blood selenium and zinc concentrations, antioxidant capacities, and intestinal microflora in canine. Biol Trace Elem Res 141(1–3):170–183

    Article  CAS  PubMed  Google Scholar 

  • Ruiz A, Poblet M, Mas A, Guillamón JM (2000) Identification of acetic acid bacteria by RFLP of PCR-amplified 16S rDNA and 16S-23S rDNA intergenic spacer. Int J Syst Evol Microbiol 50(6):1981–1987

    Article  CAS  PubMed  Google Scholar 

  • Saini K, Tomar SK, Sangwan V, Bhushan B (2014) Evaluation of lactobacilli from human sources for uptake and accumulation of selenium. Biol Trace Elem Res 160(3):433–436

    Article  CAS  PubMed  Google Scholar 

  • Samelis J, Maurogenakis F, Metaxopoulos J (1994) Characterisation of lactic acid bacteria isolated from naturally fermented Greek dry salami. Int J Food Microbiol 23(2):179

    Article  CAS  PubMed  Google Scholar 

  • Sarang DP, Poonam PS, Hitesh K, Sudhir KT, Rameshwar S (2014) Selenium enrichment of lactic acid bacteria and bifidobacteria: a functional food perspective. Trends Food Sci Technol 39:135–145

    Article  CAS  Google Scholar 

  • Shakibaie M, Mohammadi-Khorsand T, Adeli-Sardou M, Jafari M, Amirpour-Rostami S, Ameri A, Forootanfar H (2017) Probiotic and antioxidant properties of selenium-enriched Lactobacillus brevis LSe isolated from an Iranian traditional dairy product. J Trace Elem Med Bio 40:1–9

    Article  CAS  Google Scholar 

  • Simic MG (1988) Mechanisms of inhibition of free-radical processes in mutagenesis and carcinogenesis. Mutat Res 202(2):377–386

    Article  CAS  PubMed  Google Scholar 

  • Simmons AE, Karimi I, Talwar M, Simmons TW (2012) Effects of nitrite on development of embryos and early larval stages of the Zebrafish (Danio rerio). Zebrafish 9(4):200–206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sohn CH, Seo DW, Ryoo SM, Lee JH, Kim WY, Lim KS, Oh BJ (2014) Life-threatening methemoglobinemia after unintentional ingestion of antifreeze admixtures containing sodium nitrite in the construction sites. Clin Toxicol 52(1):44–47

    Article  CAS  Google Scholar 

  • Steinbrenner H, Sies H (2013) Selenium homeostasis and antioxidant selenoproteins in brain: implications for disorders in the central nervous system. Arch Biochem Biophys 536(2):152–157

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor KACC (1996) A simple colorimetric assay for muramic acid and lactic acid. Appl Biochem Biotech 56(1):49–58

    Article  CAS  Google Scholar 

  • Wang Y, Fu L (2012) Forms of selenium affect its transport, uptake and glutathione peroxidase activity in the Caco-2 cell model. Biol Trace Elem Res 149(1):110

    Article  CAS  PubMed  Google Scholar 

  • Wang XH, Ren HY, Liu DY, Zhu WY, Wang W (2013) Effects of inoculating Lactobacillus sakei starter cultures on the microbiological quality and nitrite depletion of Chinese fermented sausages. Food Control 32(2):591–596

    Article  CAS  Google Scholar 

  • Wang YQ, Wu YY, Li LH, Wang XC, Cai QX, Yang XQ (2015) Comparative study of eight strains of lactic acid bacteria in vitro antioxidant activity. Adv Mater Res 1073–1076:183–188

    Google Scholar 

  • Wolf G, Hammes WP (1988) Effect of hematin on the activities of nitrite reductase and catalase in lactobacilli. Arch Microbiol 149(3):220–224

    Article  CAS  Google Scholar 

  • Wu ZQ, Yue GZ, Zhu QP, Jiang YJ, Tang KY, Chen HP (2015) Purification, dynamic changes and antioxidant activities of oleuropein in olive (olea europaea l.) leaves. J Food Biochem 39(5):566–574

    Article  CAS  Google Scholar 

  • Xia SK, Chen L, Liang JQ (2007) Enriched selenium and its effects on growth and biochemical composition in Lactobacillus bulgaricus. J Agr Food Chem 55(6):2413–2417

    Article  CAS  Google Scholar 

  • Yan PM, Xue WT, Tan SS, Zhang H, Chang XH (2008) Effect of inoculating lactic acid bacteria starter cultures on the nitrite concentration of fermenting Chinese paocai. Food Control 19(1):50–55

    Article  CAS  Google Scholar 

  • Zeng H, Cao JJ Jr CGF (2013) Selenium in bone health: roles in antioxidant protection and cell proliferation. Nutrients 5(1):97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang BW, Kang Z, Zhang JL, Qian C, Liu GR, Nan S, Lin FX (2009) Accumulation and species distribution of selenium in Se-enriched bacterial cells of the Bifidobacterium animalis 01. Food Chem 115(2):727–734

    Article  CAS  Google Scholar 

  • Zhang L, Liu C, Li D, Zhao Y, Zhang X, Zeng X, Li S (2013) Antioxidant activity of an exopolysaccharide isolated from Lactobacillus plantarum C88. Int J Biol Macromol 54(1):270

    PubMed  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (No: 31601455).

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  1. Yang Chen and Qin Li have contributed equally to this work.

Authors and Affiliations

  1. Research Center of Food Fermentation Engineering and Technology of Hubei, Department of Bioengineering and Food Science, Hubei Cooperative Innovation Center for Industrial Fermentation, Hubei University of Technology, No. 28, Nanli Road, Hongshan District, Wuhan, 430068, Hubei Province, China

    Yang Chen, Qin Li, Chengcheng Xia, Fan Yang, Ning Xu, Qian Wu, Yong Hu, Chao Wang & Mengzhou Zhou

  2. Department of gastroenterology, Renmin Hospital of Wuhan University, Wuhan, 430068, China

    Lusha Xia

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  1. Yang Chen
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Chen, Y., Li, Q., Xia, C. et al. Effect of selenium supplements on the antioxidant activity and nitrite degradation of lactic acid bacteria. World J Microbiol Biotechnol 35, 61 (2019). https://doi.org/10.1007/s11274-019-2609-x

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