Skip to main content

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

Abstract

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. 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

    Book  Google Scholar 

  2. 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

    CAS  Article  PubMed  Google Scholar 

  3. 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

    Chapter  Google Scholar 

  4. 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

    Article  PubMed  PubMed Central  Google Scholar 

  5. 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

    CAS  Article  PubMed  Google Scholar 

  6. 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

    Book  Google Scholar 

  7. 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

    CAS  Article  PubMed  Google Scholar 

  8. 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

    CAS  Article  PubMed  Google Scholar 

  9. 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

    CAS  Article  Google Scholar 

  10. 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

    CAS  Article  PubMed  Google Scholar 

  11. 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

    CAS  Article  Google Scholar 

  12. 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

    CAS  Article  Google Scholar 

  13. 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

    CAS  Article  PubMed  Google Scholar 

  14. 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

    CAS  Article  PubMed  Google Scholar 

  15. 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

    CAS  Article  PubMed  Google Scholar 

  16. 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

    CAS  Article  Google Scholar 

  17. 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

    CAS  Article  PubMed  Google Scholar 

  18. 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

    CAS  Article  PubMed  Google Scholar 

  19. 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

    CAS  Article  PubMed  Google Scholar 

  20. 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

    CAS  Article  Google Scholar 

  21. 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

    CAS  Article  Google Scholar 

  22. 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

    CAS  Article  Google Scholar 

  23. 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

    Article  PubMed  Google Scholar 

  24. 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

    CAS  Article  PubMed  Google Scholar 

  25. 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

    Article  PubMed  PubMed Central  Google Scholar 

  26. 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

    CAS  Article  PubMed  Google Scholar 

  27. 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

    CAS  Article  PubMed  Google Scholar 

  28. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. 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

    CAS  Article  PubMed  Google Scholar 

  30. 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

    CAS  Article  PubMed  Google Scholar 

  31. 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

    CAS  Article  PubMed  Google Scholar 

  32. 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

    CAS  Article  PubMed  Google Scholar 

  33. 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

    CAS  Article  Google Scholar 

  34. 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

    Chapter  Google Scholar 

  35. 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

    CAS  Article  Google Scholar 

  36. 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

  37. 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

    CAS  Article  PubMed  Google Scholar 

  38. 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

    CAS  Article  Google Scholar 

  39. 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

    CAS  Article  PubMed  Google Scholar 

  40. Kitajima T, Chiba Y (2013) Selenomethionine metabolism and its toxicity. Biomol Concepts 4(6):611–616. https://doi.org/10.1515/bmc-2013-0033

    CAS  Article  PubMed  Google Scholar 

  41. 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

    CAS  Article  Google Scholar 

  42. 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

    CAS  Article  Google Scholar 

  43. 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

    CAS  Article  PubMed  Google Scholar 

  44. 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

    CAS  Article  Google Scholar 

  45. 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

    Article  Google Scholar 

  46. 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

    CAS  Article  PubMed  Google Scholar 

  47. 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

    CAS  Article  PubMed  Google Scholar 

  48. 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

    CAS  Article  Google Scholar 

  49. 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

    CAS  Article  PubMed  Google Scholar 

  50. Ganther HE (1986) Pathways of selenium metabolism including respiratory excretory products. Int J Toxicol 5(1):1–5. https://doi.org/10.3109/10915818609140731

    CAS  Article  Google Scholar 

  51. 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

    CAS  Article  Google Scholar 

  52. 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

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Special Fund for Agro-scientific Research in the Public Interest (201303106), the National Natural Science Foundation of China (31470531), the Program for Liaoning Excellent Talents in University (LR2015058), and the Scientific Research Foundation for the Introduced Talents of Shenyang Agricultural University (20153040).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yanbin Guo.

Electronic Supplementary Material

Figure S1
figure 6

Biomass production in fruiting bodies treated with different concentrations of selenate [Se (VI)], selenite [Se (IV)], or selenomethionine (SeMet). Control treatments lacked Se in the medium. Data are mean ± SD (n = 3). Different letters (a, b, c…) indicate significant differences among Se treatments (p < 0.05). (GIF 39 kb)

High resolution image (TIF 18081 kb)

Table S1

(DOCX 42 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hu, T., Liang, Y., Zhao, G. et al. Selenium Biofortification and Antioxidant Activity in Cordyceps militaris Supplied with Selenate, Selenite, or Selenomethionine. Biol Trace Elem Res 187, 553–561 (2019). https://doi.org/10.1007/s12011-018-1386-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-018-1386-y

Keywords

  • Antioxidant
  • Biofortification
  • Cordyceps militaris
  • Cordycepin
  • Selenium