Abstract
The accumulation of selenium (Se) by Lactobacillus delbrueckii ssp. bulgaricus (Lb) and Streptococcus thermophilus (St) at the different cultivation conditions, including initial pH, inoculum dose (%), and temperature (°C), was investigated in this work. Se enrichment efficiency was optimized using the Design-Expert software for response surface methodology on a basis of single-factor experiment. The antioxidant activities of Se-enriched Lactic acid bacteria (LAB) were also investigated. The qualitative analysis of Se-enriched LAB was performed by FT-IR spectra. The cell morphology and chemical element components were measured by a scanning electron microscope (SEM) equipped with energy-dispersive X-ray spectroscopy. The results indicated that the optimum initial pH, inoculum doses, and temperatures of Lb and St were 5.96, 6.73%, 33.24 °C, and 6.37, 6%, 40 °C, respectively. Under the optimal conditions, the ratios of Se enrichment reached 94.34% for Lb and 97.05% for St. Furthermore, Se-enriched LAB enhanced scavenging rates on DPPH, ABTS free radical, and also heightened reducing activity. The FT-IR results showed that the two Se-enriched strains had similar characteristic absorption peaks, which were further demonstrated that both Se biomasses had the same carbonyl, carboxyl, and hydroxyl groups. Elemental selenium nanoparticles were verified around cell surfaces of Se-enriched LAB, which implied that both strains had detoxification ability when grown in liquid media containing selenite.
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References
Ahmad AA, Hameed BH (2010) Effect of preparation conditions of activated carbon from bamboo waste for real textile wastewater. J Hazard Mater 173:487–493. doi:10.1016/j.jhazmat.2009.08.111
Andreoni V, Luischi MM, Cavalca L, Erba D, Ciappellano S (2000) Selenite tolerance and accumulation in the Lactobacillus species. Ann Microbiol 50:77–88
Anupam K, Dutta S, Bhattacharjee C, Datta S (2011) Adsorptive removal of chromium (VI) from aqueous solution over powdered activated carbon: optimisation through response surface methodology. Chem Eng J 173:135–143. doi:10.1016/j.cej.2011.07.049
Bajaj M, Schmidt S, Winter J (2012) Formation of Se (0) Nanoparticles by Duganella sp and Agrobacterium sp. isolated from Se-laden soil of North-East Punjab, India. Microb Cell Fact 11:64. doi:10.1186/1475-2859-11-64
Benko I et al (2012) Subacute toxicity of nano-selenium compared to other selenium species in mice. Environ Toxicol Chem 31:2812–2820. doi:10.1002/etc.1995
Deng Y et al (2015) Preparation of elemental selenium-enriched fermented milk by newly isolated Lactobacillus brevis from kefir grains. Int Dairy J 44:31–36. doi:10.1016/j.idairyj.2014.12.008
Drutel A, Archambeaud F, Caron P (2013) Selenium and the thyroid gland: more good news for clinicians. Clin Endocrinol 78:155–164
Dumont E, Vanhaecke F, Cornelis R (2006) Selenium speciation from food source to metabolites: a critical review. Anal Bioanal Chem 385:1304–1323. doi:10.1007/s00216-006-0529-8
Galano E et al (2013) Privileged incorporation of selenium as selenocysteine in Lactobacillus reuteri proteins demonstrated by selenium-specific imaging and proteomics. Mol Cell Proteom 12:2196–2204. doi:10.1074/mcp.M113.027607
Gao XJ, Zhang ZC, Li Y, Shen P, Hu XY, Cao YG, Zhang NS (2016) Selenium deficiency facilitates inflammation following S. aureus infection by regulating TLR2-related pathways in the mouse mammary gland. Biol Trace Elem Res 172:449–457. doi:10.1007/s12011-015-0614-y
Garbisu C, Ishii T, Leighton T, Buchanan BB (1996) Bacterial reduction of selenite to elemental selenium. Chem Geol 132:199–204. doi:10.1016/s0009-2541(96)00056-3
Gole A, Dash C, Ramakrishnan V, Sainkar SR, Mandale AB, Rao M, Sastry M (2001) Pepsin-gold colloid conjugates: preparation, characterization, and enzymatic activity. Langmuir 17:1674–1679. doi:10.1021/la001164w
Hnain A, Brooks J, Lefebvre DD (2013) The synthesis of elemental selenium particles by Synechococcus leopoliensis. Appl Microbiol Biotechnol 97:10511–10519. doi:10.1007/s00253-013-5304-0
Jimenez-Cedillo MJ, Olguin MT, Fall C, Colin-Cruz A (2013) As(III) and As(V) sorption on iron-modified non-pyrolyzed and pyrolyzed biomass from Petroselinum crispum (parsley). J Environ Manag 117:242–252. doi:10.1016/j.jenvman.2012.12.023
Kessi J, Hanselmann KW (2004) Similarities between the abiotic reduction of selenite with glutathione and the dissimilatory reaction mediated by Rhodospirillum rubrum and Escherichia coli. J Biol Chem 279:50662–50669. doi:10.1074/jbc.M405887200
Kieliszek M, Blazejak S (2013) Selenium: significance, and outlook for supplementation. Nutrition 29:713–718. doi:10.1016/j.nut.2012.11.012
Kieliszek M, Blazejak S (2016) Current knowledge on the importance of selenium in food for living organisms: a review. Molecules 21:609. doi:10.3390/molecules21050609
Kieliszek M, Blazejak S, Gientka I, Bzducha-Wrobel A (2015) Accumulation and metabolism of selenium by yeast cells. Appl Microbiol Biotechnol 99:5373–5382. doi:10.1007/s00253-015-6650-x
Kieliszek M, Blazejak S, Bzducha-Wrobel A, Kurcz A (2016a) Effects of selenium on morphological changes in Candida utilis ATCC 9950 yeast cells. Biol Trace Elem Res 169:387–393. doi:10.1007/s12011-015-0415-3
Kieliszek M, Blazejak S, Placzek M (2016b) Spectrophotometric evaluation of selenium binding by Saccharomyces cerevisiae ATCC MYA-2200 and Candida utilis ATCC 9950 yeast. J Trace Elem Med Biol 35:90–96. doi:10.1016/j.jtemb.2016.01.014
Kim YS, Milner J (2001) Molecular targets for selenium in cancer prevention. Nutr Cancer Int J 40:50–54. doi:10.1207/s15327914nc401_10
Li X, Liu Y, Wu J, Liang HG, Qu SS (2002) Microcalorimetric study of Staphylococcus aureus growth affected by selenium compounds. Thermochim Acta 387:57–61
Lin MY, Chang FJ (2000) Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356. Dig Dis Sci 45:1617–1622. doi:10.1023/a:1005577330695
Lin MY, Yen CL (1999) Antioxidative ability of lactic acid bacteria. J Agric Food Chem 47:1460–1466. doi:10.1021/jf981149l
Lin ZY, Wu JM, Xue R, Yang Y (2005) Spectroscopic characterization of Au3+ biosorption by waste biomass of Saccharomyces cerevisiae. Spectrochim Acta A 61:761–765. doi:10.1016/j.saa.2004.03.029
Mater DDG, Bretigny L, Firmesse O, Flores MJ, Mogenet A, Bresson JL, Corthier G (2005) Streptococcus thermophilus and Lactobacillus delbrueckii subsp bulgaricus survive gastrointestinal transit of healthy volunteers consuming yogurt. Fems Microbiol Lett 250:185–187. doi:10.1016/j.femsle.2005.07.006
Mogna L, Nicola S, Pane M, Lorenzini P, Strozzi G, Mogna G (2012) Selenium and zinc internalized by Lactobacillus buchneri Lb26 (DSM 16341) and Bifidobacterium lactis Bb1 (DSM 17850): improved bioavailability using a new biological approach. J Clin Gastroenterol 46:S41–S45
Monsen ER (2000) Dietary reference intakes for the antioxidant nutrients: vitamin C, vitamin E, selenium, and carotenoids. J Am Diet Assoc 100:637–640. doi:10.1016/S0002-8223(00)00189-9
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 J Microbiol Biotechnol 28:2771–2782. doi:10.1007/s11274-012-1094-2
Navarro-Alarcon M, Lopez-Martinez MC (2000) Essentiality of selenium in the human body: relationship with different diseases. Sci Total Environ 249:347–371. doi:10.1016/s0048-9697(99)00526-4
Nelson DC, Casey WH, Sison JD, Mack EE, Ahmad A, Pollack JS (1996) Selenium uptake by sulfur-accumulating bacteria. Geochimica et Cosmochimica Acta 60:3531–3539. doi:10.1016/0016-7037(96)00221-9
Nuttall KL (2006) Evaluating selenium poisoning. Ann Clin Lab Sci 36:409–420
Penas E et al (2012) Se improves indole glucosinolate hydrolysis products content Se-methylselenocysteine content, antioxidant capacity and potential anti-inflammatory properties of sauerkraut. Food Chem 132:907–914. doi:10.1016/j.foodchem.2011.11.064
Pieniz S, Andreazza R, Anghinoni T, Camargo F, Brandelli A (2014) Probiotic potential, antimicrobial and antioxidant activities of Enterococcus durans strain LAB18s. Food Control 37:251–256. doi:10.1016/j.foodcont.2013.09.055
Reid G, Burton J (2002) Use of Lactobacillus to prevent infection by pathogenic bacteria. Microbes Infect 4:319–324. doi:10.1016/s1286-4579(02)01544-7
Sayilgan E, Cakmakci O (2013) Treatment of textile dyeing wastewater by biomass of Lactobacillus: lactobacillus 12 and Lactobacillus rhamnosus. Environ Sci Pollut Res 20:1556–1564. doi:10.1007/s11356-012-1009-7
Schut S, Zauner S, Hampel G, Koenig H, Claus H (2011) Biosorption of copper by wine-relevant lactobacilli. Int J Food Microbiol 145:126–131. doi:10.1016/j.ijfoodmicro.2010.11.039
Selatnia A, Boukazoula A, Kechid N, Bakhti MZ, Chergui A (2004) Biosorption of Fe3+ from aqueous solution by a bacterial dead Streptomyces rimosus biomass. Process Biochem 39:1643–1651. doi:10.1016/s0032-9592(03)00305-4
Sofu A, Sayilgan E, Guney G (2015) Experimental design for removal of Fe(II) and Zn(II) ions by different lactic acid bacteria biomasses. Int J Environ Res 9:93–100
Suhajda A, Hegoczki J, Janzso B, Pais I, Vereczkey G (2000) Preparation of selenium yeasts I. Preparation of selenium-enriched Saccharomyces cerevisiae. J Trace Elem Med Biol 14:43–47. doi:10.1016/s0946-672x(00)80022-x
Suzuki KT, Kurasaki K, Ogawa S, Suzuki N (2006) Metabolic transformation of methylseleninic acid through key selenium intermediate selenide. Toxicol Appl Pharmacol 215:189–197
Tahmouzi S (2014) Optimization of polysaccharides from Zagros oak leaf using RSM: antioxidant and antimicrobial activities. Carbohydr Polym 106:238–246. doi:10.1016/j.carbpol.2014.02.028
Tan G, Yuan H, Liu Y, Xiao D (2010) Removal of lead from aqueous solution with native and chemically modified corncobs. J Hazard Mater 174:740–745. doi:10.1016/j.jhazmat.2009.09.114
Ungvari E et al (2014) Protective effects of meat from lambs on selenium nanoparticle supplemented diet in a mouse model of polycyclic aromatic hydrocarbon-induced immunotoxicity. Food Chem Toxicol 64:298–306. doi:10.1016/j.fct.2013.12.004
Veneu DM, Torem ML, Pino GAH (2013) Fundamental aspects of copper and zinc removal from aqueous solutions using a Streptomyces lunalinharesii strain. Miner Eng 48:44–50. doi:10.1016/j.mineng.2012.11.015
Wang LF (2007) Determination of trace selenium in organic samples. Food Machin 23(1):115
Wang J, Chen C (2009) Biosorbents for heavy metals removal and their future. Biotechnol Adv 27:195–226. doi:10.1016/j.biotechadv.2008.11.002
Wang J, Zhao X, Yang Y, Zhao A, Yang Z (2015) Characterization and bioactivities of an exopolysaccharide produced by Lactobacillus plantarum YW32. Int J Biol Macromol 74:119–126. doi:10.1016/j.ijbiomac.2014.12.006
Wootton-Beard PC, Moran A, Ryan L (2011) Stability of the total antioxidant capacity and total polyphenol content of 23 commercially available vegetable juices before and after in vitro digestion measured by FRAP, DPPH, ABTS and Folin-Ciocalteu methods. Food Res Int 44:217–224. doi:10.1016/j.foodres.2010.10.033
Xia SK, Chen L, Liang JQ (2007) Enriched selenium and its effects on growth and biochemical composition in Lactobacillus bulgaricus. J Agric Food Chem 55:2413–2417. doi:10.1021/jf062946j
Ye S, Zhang J, Liu Z, Zhang Y, Li J, Li YO (2016) Biosynthesis of selenium rich exopolysaccharide (Se-EPS) by Pseudomonas PT-8 and characterization of its antioxidant activities. Carbohydr Polym 142:230–239. doi:10.1016/j.carbpol.2016.01.058
Zhai Q et al (2015) Screening of lactic acid bacteria with potential protective effects against cadmium toxicity. Food Control 54:23–30. doi:10.1016/j.foodcont.2015.01.037
Zhang ES, Wang HL, Yan XX, Zhang LD (2005) Comparison of short-term toxicity between Nano-Se and selenite in mice. Life Sci 76:1099–1109. doi:10.1016/j.lfs.2004.08.015
Zhang GC, Wang DH, Wang DH, Wei GY (2016) The mechanism of improved intracellular organic selenium and glutathione contents in selenium-enriched candida utilis, by acid stress. Appl Microbiol Biotechnol 101(5):2131. doi:10.1007/s00253-016-8016-4
Zhu ZJ, Jiang WQ, Ganther HE, Ip C, Thompson HJ (2000) Activity of se-allylselenocysteine in the presence of methionine gamma-lyase on cell growth. DNA integrity, apoptosis, and cell-cycle regulatory molecules. Mol Carcinog 29:191–197. doi:10.1002/1098-2744(200012)29:4<191:aid-mc1000>3.0.co;2-7
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This work was supported by the Grant No. 2016NY-148 from the Department of Science & Technology of Shaanxi Province.
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Yang, J., Li, Y., Zhang, L. et al. Response surface design for accumulation of selenium by different lactic acid bacteria. 3 Biotech 7, 52 (2017). https://doi.org/10.1007/s13205-017-0709-6
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DOI: https://doi.org/10.1007/s13205-017-0709-6