Selenium Biofortification and Antioxidant Activity in Cordyceps militaris Supplied with Selenate, Selenite, or Selenomethionine

Biological Trace Element Research - Tập 187 - Trang 553-561 - 2018
Ting Hu1,2, Yue Liang3, Guishen Zhao1,2, Wenliang Wu1,2, Huafen Li1,2, Yanbin Guo1,2
1College of Resources and Environmental Sciences, China Agricultural University, Beijing, China
2Beijing Key Laboratory of Biodiversity and Organic Farming, China Agricultural University, Beijing, China
3College of Plant Protection, Shenyang Agricultural University, Shenyang, China

Tóm tắt

Selenium (Se) is an essential trace element with multiple functions that may help mitigate adverse health conditions. Cordyceps militaris is an edible mushroom with medicinal properties. The experiment was conducted under artificial cultivation, with five Se concentrations (0, 5, 10, 20, and 40 μg g−1) and three forms of Se (selenate, selenite, and selenomethionine). C. militaris can absorb inorganic from the substrate and convert it to organic Se compounds (selenocystine, selenomethionine, and an unknown species) in fruiting bodies. Compared with the control treatment, Se applications (40 μg g−1 selenate and selenite) significantly increased the Se concentration in fruiting bodies by 130.9 and 128.1 μg g−1, respectively. The biofortification with selenate and selenite did not affect fruiting body production, in some case, but did enhance the biological efficiency. Moreover, the abundance of cordycepin and adenosine increased, while the amino acid contents remained relatively stable. Meanwhile, Se-biofortified C. militaris showed effective antioxidant activities. These results suggest that Se-biofortified C. militaris fruiting bodies may enhance human and animal health when it was included as part of a healthy diet or used as Se supplements.

Tài liệu tham khảo

Reilly C (2006) Selenium in food and health, 2nd edn. Springer, New York, pp 20–40. https://doi.org/10.1007/978-0-387-33244-4 Fairweather-Tait SJ, Bao YP, Broadley MR, Collings R, Ford D, Ford D, Hesketh JE, Hurst R (2011) Selenium in human health and disease. Antioxid Redox Signal 14(7):1337–1383. https://doi.org/10.1089/ars.2010.3275 Fordyce FM (2013) Selenium deficiency and toxicity in the environment. In: Selinus O (ed) Essentials of medical geology. Springer, Dordrecht, pp 375–415. https://doi.org/10.1007/978-94-007-4375-5_16 Stranges S, Sieri S, Vinceti M, Grionic S, Guallar E, Laclaustra M, Muti P, Berrino F, Krogh V (2010) A prospective study of dietary selenium intake and risk of type 2 diabetes. BMC Public Health 10(1):564. https://doi.org/10.1186/1471-2458-10-564 Tanguy S, Grauzam S, Leiris J, Boucher F (2012) Impact of dietary selenium intake on cardiac health: experimental approaches and human studies. Mol Nutr Food Res 56(7):1106–1121. https://doi.org/10.1002/mnfr.201100766 Food and Nutrition Board (2000) Dietary reference intakes for vitamin C, vitamin E, selenium, and carotenoids. Institute of Medicine, National Academic Press, Washington, DC. https://doi.org/10.17226/9810 Arnault I, Auger J (2006) Seleno-compounds in garlic and onion. J Chromatogr A 1112(1–2):23–30. https://doi.org/10.1016/j.chroma.2006.01.036 Weekley CM, Harris HH (2013) Which form is that? The importance of selenium speciation and metabolism in the prevention and treatment of disease. Chem Soc Rev 42(23):8870–8894. https://doi.org/10.1039/c3cs60272a EI-Ramady HR, Domokos-Szabolcsy É, Abdalla NA, Alshaal TA, Shalaby TA, Sztrik A, Prokisch J, Fári M (2014) Selenium and nono-selenium in agroecosystems. Environ Chem Lett 12(4):495–510. https://doi.org/10.1007/s10311-014-0476-0 Wang YD, Wang X, Wong YS (2013) Generation of selenium-enriched rice with enhanced grain yield, selenium content and bioavailability through fertilization with selenite. Food Chem 141(3):2385–2393. https://doi.org/10.1016/j.foodchem.2013.05.095 Burk RF, Norsworthy BK, Hill KE, Motley AK, Byrne DW (2006) Effects of chemical form of selenium on plasma biomarkers in a high-dose human supplementation trial. Cancer Epidemiol Biomark Prev 15(4):804–810. https://doi.org/10.1158/1055-9965.EPI-05-0950 Barger JL, Kayo T, Pugh TD, Vann JA, Power R, Dawson K, Weindruch R, Prolla TA (2012) Gene expression profiling reveals differential effects of sodium selenite, selenomethionine, and yeast-deriver selenium in mouse. Genes Nutr 7(2):155−165–155−165. https://doi.org/10.1007/s12263-011-0243-9 Dumont E, Vanhaecke F, Cornelis R (2006) Selenium speciation from food source to metabolites: a critical review. Anal Bioanal Chem 385(7):1304–1323. https://doi.org/10.1007/s00216-006-0529-8 Hartikainen H (2005) Biogeochemistry of selenium and its impact on food chain quality and human health. J Trace Elem Med Biol 18(4):309–318. https://doi.org/10.1016/j.jtemb.2005.02.009 Bhatia P, Aureli F, D’Amato M, Prakash R, Cameotra SS, Nagaraja TP, Cubadda F (2013) Selenium bioaccessibility and speciation in biofortified Pleurotus mushrooms grown on selenium-rich agricultural residues. Food Chem 140(1–2):225–230. https://doi.org/10.1016/j.foodchem.2013.02.054 da Silva MCS, Naozuka J, da Luz JMR, de Assunção LS, Oliveira PV, Vanetti MCD, Bazzolli DMS, Kasuya MCM (2012) Enrichment of Pleurotus ostrestus mushrooms with selenium in coffee husks. Food Chem 131(2):558–563. https://doi.org/10.1016/j.foodchem.2011.09.023 Maseko T, Callahan DL, Dunshea FR, Doronila A, Kolev SD, Ng K (2013) Chemical characterization and speciation of organic selenium in cultivated selenium-enriched Agaricus bisporus. Food Chem 141(4):3681–3687. https://doi.org/10.1016/j.foodchem.2013.06.027 Rzymski P, Mleczek M, Niedzielski P, Siwulski M, Gąsecka M (2016) Potential of cultivated Ganoderma lucidum mushrooms for the production of supplements enriched with essential elements. J Food Sci 81(3):C587–C582. https://doi.org/10.1111/1750-3841.13212 Rzymski R, Mleczek M, Niedzielski P, Siwulski M, Gąsecka M (2016) Cultivation of Agaricus bisporus, enriched with selenium, zinc and copper. J Sci Food Agric 97(3):923–928. https://doi.org/10.1002/jsfa.7816 Niedzielski P, Mleczek M, Siwulski M, Rzymski P, Gasecka M, Kozak L (2015) Supplementation of cultivated mushroom species with selenium: bioaccumulation and speciation study. Eur Food Res Technol 241(3):419–426. https://doi.org/10.1007/s00217-015-2474-2 Poniedziałek B, Mleczek M, Niedzielski P, Siwulski M, Gąsecka M, Kozak L, Komosa A, Rzymski P (2017) Bio-enriched Pleurotus mushrooms for deficiency control and improved antioxidative protection of human platelets? Eur Food Res Technol 243(12):2187–2198. https://doi.org/10.1007/s00217-017-2921-3 Paterson RRM (2008) Cordyceps—a traditional Chinese medicine fungal therapeutic biofactory? Phytochemistry 39(31):1469–1495. https://doi.org/10.1016/j.phytochem.2008.01.027 Das SK, Masuda M, Sakurai A, Sakakibara M (2010) Medicinal uses of the mushroom Cordyceps militaris: current state and prospects. Fitoterapia 81(8):961–968. https://doi.org/10.1016/j.fitote.2010.07.010 Arnold MC, Lindberg TT, Liu YT, Porter KA, Hsu-Kim H, Hinton DE, Giulio RTD (2014) Bioaccumulation and speciation of selenium in fish and insects collected from a mountaintop removal coal mining-impacted stream in West Virgina. Ecotoxicology 23(5):929–938. https://doi.org/10.1007/s10646-014-1236-4 Sung GH, Hywel-Jones NL, Sung JM, Luangsa-Ard JJ, Shrestha B, Spatafora JW (2007) Phylogenetic classification of Cordyceps and clavicipitaceous fungi. Stud Mycol 57(57):5–59. https://doi.org/10.3114/sim.2007.57.01 Chiu C, Liu S, Tang C, Chan Y, El-Shazly M, Lee CL, Du YC, Wu TY, Chang FR, Wu YC (2016) Anti-inflammatory cerebrosides from cultivated Cordyceps militaris. J Agric Food Chem 64(7):1540–1548. https://doi.org/10.1021/acs.jafc.5b05931 Kang HJ, Baik HW, Kim SJ, Lee SG, Ahn HY, Park JS, Park SJ, Jang EJ, Park SW, Choi JY, Sung JH, Lee SM (2015) Cordyceps militaris enhances cell-mediated immunity in healthy Korean men. J Med Food 18(10):1164–1172. https://doi.org/10.1089/jmf.2014.3350 Shao L, Huang L, Yan S, Jin J, Ren S (2016) Cordycepin induces apoptosis in human liver cancer HepG2 cells through extrinsic and intrinsic signaling pathways. Oncol Lett 12(2):995–1000. https://doi.org/10.3892/ol.2016.4706 Zhang G, Liang Y (2013) Improvement of fruiting body production in Cordyceps militaris by molecular assessment. Arch Microbiol 195(8):579–585. https://doi.org/10.1007/s00203-013-0904-8 Wang DX, Sakoda A, Suzuki M (2001) Biological efficiency and nutritional value of Pleurotus Ostreatus cultivated on spent beer grain. Bioresour Technol 78(3):293–300. https://doi.org/10.1016/S0960-8524(01)00002-5 Baldwin S, Deaker M, Maher W (1994) Low-volume microwave digestion of marine biological tissues for measurement of trace elements. Analyst 119(8):1701–1704. https://doi.org/10.1039/an9941901701 Montes-Bayón M, Molet MJD, González EB, Sanz-Medel A (2006) Evaluation of different sample extraction strategies for selenium determination in selenium-enriched plants (Allium sativum and Brassica juncea) and Se speciation by HPLC-ICP-MS. Talanta 68(4):1287–1293. https://doi.org/10.1016/j.talanta.2005.07.040 Li JM, Guan MY, Li Y (2015) Effects of cooking on the contents of adenosine and cordycepin in Cordyceps militaris. Procedia Eng 102:485–491. https://doi.org/10.1016/j.proeng.2015.01.195 Oser BL (1959) An integrated essential amino acid index for predicting the biological value of proteins. In: Albanese AA (ed) Protein and amino acids in nutrition. Academic Press, New York, pp 281–295. https://doi.org/10.1016/B978-0-12-395683-5.50014-6 Cheung LM, Cheung PCK, Ooi VEC (2003) Antioxidant activity and total phenolics edible mushroom extracts. Food Chem 81(2):249–255. https://doi.org/10.1016/S0308-8146(02)00419-3 de Souza MP, Pilon-Smits EAH, Lytle CM, Hwang S, Tai HJ, Honma TS, Yeh L, Terry N (1998) Rate-limiting steps in selenium assimilation and volatilization by Indian mustard. Plant Physiol. 117(4):1487–1494. https://doi.org/10.1104/pp.117.4.1487 Sors TG, Ellis DR, Salt DE (2005) Selenium uptake, translocation, assimilation and metabolic fate in plants. Photosynth Res 86(3):373–389. https://doi.org/10.1007/s11120-005-5222-9 Egressy-Molnár O, Ouerdane L, Győrfi J, Dernovics M (2016) Analogy in selenium enrichment and selenium speciation between selenized yeast Saccharomyces cerevisiae and Hericuium erinaceus (Lion’s mane mushroom). LWT - Food Sci Technol 68:306–312. https://doi.org/10.1016/j.lwt.2015.12.028 Schrauzer GN (2000) Selenomethionine: a review of it nutritional significance metabolism and toxicity. J Nutr 130(7):1653–1656. https://doi.org/10.1093/jn/130.7.1653 Kitajima T, Chiba Y (2013) Selenomethionine metabolism and its toxicity. Biomol Concepts 4(6):611–616. https://doi.org/10.1515/bmc-2013-0033 Zhang H, Zhang H, Han L, Wang S (2014) Cultivation technique of selenium-enriched Cordyceps militaris. Appl Mech Mater 522–524:1147–1150. https://doi.org/10.4028/www.scientific.net/AMM.522-524.1147 Fan DD, Wang W, Zhong JJ (2012) Enhancement of cordycepin production in submerged cultures of Cordyceps militaris by addition of ferrous sulfate. Biochem Eng J 60(2):30–35. https://doi.org/10.1016/j.bej.2011.09.014 Kredich NM, Guarino AJ (1961) Studies on the biosynthesis of cordycepin. Biochim Biophys Acta 47(3):529–534. https://doi.org/10.1016/0006-3002(61)90546-7 Turlo J, Gutkowska B, Herold F (2010) Effect of selenium enrichment on antioxidant activities and chemical composition of Lentinula edodes (Berk.) Pegl. Mycelia extracts. Food Chem Toxicol 48(4):1085−1091–1085−1091. https://doi.org/10.1016/j.fct.2010.01.030 Peñaflorida VD (1989) An evaluation of indigenous protein sources as potential component in the diet formulation for tiger prawn, Penaeus monodon, using essential amino acid index (EAAI). Aquaculture 83(3–4):319–330. https://doi.org/10.1016/0044-8486(89)90043-4 Cho J, Kang JS, Long PH, Jing J, Back Y, Chung KS (2003) Antioxidant and memory enhancing effects of purple sweet potato anthocyanin and cordyceps mushroom extract. Arch Pharm Res 26(10):821–825. https://doi.org/10.1007/BF02980027 Li SP, Li P, Dong TTX, Tsim KWK (2001) Anti-oxidation activity of different types of natural Cordyceps sinensis and cultured Cordyceps mycelia. Phytomedicine 8(3):207–212. https://doi.org/10.1078/0944-7113-00030 Reis FS, Martins A, Barros L, Ferreira ICFR (2002) Antioxidant properties and phenolic profile of the most widely appreciated cultivated mushrooms: a comparative study between in vivo and vitro samples. Food Chem Toxicol 50(5):1201–1207. https://doi.org/10.1016/j.fct.2012.02.013 Rotruck JT, Pope AL, Ganther HE, Swanson AB, Hafeman DG, Hoekstra WG (1973) Selenium: biochemical role as a component of glutathione peroxidase. Science 179:588–590. https://doi.org/10.1126/science.179.4073.588 Ganther HE (1986) Pathways of selenium metabolism including respiratory excretory products. Int J Toxicol 5(1):1–5. https://doi.org/10.3109/10915818609140731 Jacob C, Giles GI, Giles NM, Sies H (2003) Sulfur and selenium: the role of oxidation state in protein structure and function. Angew Chem Int Ed 42(39):4742–4758. https://doi.org/10.1002/anie.200300573 Wu J, Lyons GH, Graham RD, Fenech MF (2009) The effect of selenium, as selenomethionine, on genome stability and cytotoxicity in human lymphocytes measured using the cytokinesis-block micronucleus cytome assay. Mutagenesis 24(3):225–232. https://doi.org/10.1093/mutage/gen074