Mechanisms into the removal and translocation of cadmium by Oudemansiella radicata in soil

  • Xuedan Li
  • Kemeng Xiao
  • Hang Ma
  • Lingling Li
  • Hang Tan
  • Heng Xu
  • Yunzhen Li
Research Article


This study investigated the removal and translocation mechanism of cadmium (Cd) by Oudemansiella radicata (O. radicata) in mushroom-soil rhizosphere and the fruiting body of mushroom. For this, the biomass, physiochemical parameters, and Cd distribution of O. radicata were examined in the soil spiked with 0, 10, 20, and 30 mg kg−1 Cd. The soil microecology and the Cd fractionation in the soil rhizosphere were also measured. Results showed that, O. radicata possesses high capability to tolerate Cd, although its surface phenotypic structure was influenced by high concentrations of Cd. The observed concentrations of Cd in O. radicata were in the following order: root (the part of stipe in soil) > pileus > stipe. The presence of Cd led to an increase in the production of antioxidant enzymes and glutathione (GSH). These results suggested that antioxidant enzymes and GSH assisted detoxification and accumulation of Cd within the mushroom. Meanwhile, in the soil rhizosphere, the concentrations of oxalic, citric, and malic acids were enhanced with the treatment of Cd, indicating that the production of these acids was closely related to the presence of Cd in soils. Additionally, the proportion of acid-soluble Cd was increased and the soil microecology (microbial counts, urease, and acid phosphatase activities) also enhanced with the inoculation of O. radicata. Overall, this study demonstrated that O. radicata is a promising candidate for the remediation of Cd-contaminated soil.


Cadmium Oudemansiella radicata Removal Translocation Mechanism Soil microecology 



The authors wish to thank Professor Guanglei Cheng and Dong Yu from Sichuan University for their technical assistance.

Funding information

The study was financially supported by the Key Research and Development Program of Sichuan Province (2017SZ0181), the Agricultural science and Technology Achievements Transformation Program of Sichuan Province (2017NZZJ008), and the NSFC (No. 41171253).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Cen F, Hu Y, Xu H (2012) Responses of antioxidant defenses in Coprinus comatus exposed to cadmium and mercury toxicity. Asian J Chem 24:4679–4685Google Scholar
  2. Chatterjee D, Datta SC, Manjaiah KM (2014) Transformation of short-range order minerals in maize (Zea mays L.) rhizosphere. Plant Soil Environ 60:241–248CrossRefGoogle Scholar
  3. Chaturvedi AD, Pal D, Penta S, Kumar A (2015) Ecotoxic heavy metals transformation by bacteria and fungi in aquatic ecosystem. World J Microbiol Biotechnol 31:1595–1603CrossRefGoogle Scholar
  4. Chen HM, Zheng CR, Tu C, Shen ZG (2000) Chemical methods and phytoremediation of soil contaminated with heavy metals. Chemosphere 41:229–234CrossRefGoogle Scholar
  5. Chen L, Luo S, Li X, Wan Y, Chen J, Liu C (2014) Interaction of Cd-hyperaccumulator Solanum nigrum L. and functional endophyte Pseudomonas sp. Lk9 on soil heavy metals uptake. Soil Biol Biochem 68:300–308CrossRefGoogle Scholar
  6. Chiang PN, Wang MK, Chiu CY, Chou SY (2010) Effects of cadmium amendments on low-molecular-weight organic acid exudates in rhizosphere soils of tobacco and sunflower. Environ Toxicol 21:479–488CrossRefGoogle Scholar
  7. Chiang PN, Chiu CY, Wang MK, Chen BT (2011) Low-molecular-weight organic acids exuded by millet (Setaria italica (L.) Beauv.) roots and their effect on the remediation of cadmium-contaminated soil. Soil Sci 176:33–38CrossRefGoogle Scholar
  8. Chivian D, Brodie EL, Alm EJ, Culley DE, Dehal PS, DeSantis TZ, Gihring TM, Lapidus A, Lin L-H, Lowry SR (2008) Environmental genomics reveals a single-species ecosystem deep within earth. Science (New York, NY) 322:275–278CrossRefGoogle Scholar
  9. Cieśliński G, Rees KCJV, Szmigielska AM, Krishnamurti GSR, Huang PM (1998) Low-molecular-weight organic acids in rhizosphere soils of durum wheat and their effect on cadmium bioaccumulation. Plant Soil 203:109–117CrossRefGoogle Scholar
  10. Collinhansen C, Andersen RA, Steinnes E (2005) Damage to DNA and lipids in Boletus edulis exposed to heavy metals. Mycol Res 109:1386–1396CrossRefGoogle Scholar
  11. Davezza M, Fabbri D, Prevot AB, Pramauro E (2011) Removal of alkylphenols from polluted sites using surfactant-assisted soil washing and photocatalysis. Environ Sci Pollut Res Int 18:783–789CrossRefGoogle Scholar
  12. Dong J, Mao WH, Zhang GP, Wu FB, Cai Y (2007) Root excretion and plant tolerance to cadmium toxicity - a review. Plant Soil Environ 53:193–200CrossRefGoogle Scholar
  13. Dresler S, Hanaka A, Bednarek W, Maksymiec W (2014) Accumulation of low-molecular-weight organic acids in roots and leaf segments of Zea mays plants treated with cadmium and copper. Acta Physiol Plant 36:1565–1575CrossRefGoogle Scholar
  14. Duarte B, Delgado M, Caçador I (2007) The role of citric acid in cadmium and nickel uptake and translocation, in Halimione portulacoides. Chemosphere 69:836–840Google Scholar
  15. Falandysz J (2016) Mercury bio-extraction by fungus Coprinus comatus: a possible bioindicator and mycoremediator of polluted soils? Environ Sci Pollut Res Int 23:7444–7451CrossRefGoogle Scholar
  16. Falandysz J, Borovička J (2013) Macro and trace mineral constituents and radionuclides in mushrooms: health benefits and risks. Appl Microbiol Biotechnol 97:477–501CrossRefGoogle Scholar
  17. Falandysz J, Mędyk M, Treu R (2018) Bio-concentration potential and associations of heavy metals in Amanita muscaria (L.) Lam. from northern regions of Poland. Environ Sci Pollut Res 25:25190–25206CrossRefGoogle Scholar
  18. Fei X, Xu L, Chen Y, Ke Z, Xu H (2016) Self-assembly modified-mushroom nanocomposite for rapid removal of hexavalent chromium from aqueous solution with bubbling fluidized bed. Sci Rep 6:26201CrossRefGoogle Scholar
  19. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefGoogle Scholar
  20. Hong J, Lei Z, Zheng B, Wang G (2012) Role of organic acids in desorption of mercury from contaminated soils in eastern Shandong Province, China. Chin Geogr Sci 22:414–421CrossRefGoogle Scholar
  21. Hui L, Na L, Li JZ, Hai MZ, Yan WL, Quan YC, Ming HW, Mo CH (2016) Do arbuscular mycorrhizal fungi affect cadmium uptake kinetics, subcellular distribution and chemical forms in rice? Sci Total Environ 571:1183–1190CrossRefGoogle Scholar
  22. Irfan M, Ahmad A, Hayat S (2014) Effect of cadmium on the growth and antioxidant enzymes in two varieties of Brassica juncea. Saudi J Biol Sci 21:125–131CrossRefGoogle Scholar
  23. Jia Z, Deng J, Chen N, Shi W, Tang X, Xu H (2016) Bioremediation of cadmium-dichlorophen co-contaminated soil by spent Lentinus edodes substrate and its effects on microbial activity and biochemical properties of soil. J Soils Sediments 17:1–11CrossRefGoogle Scholar
  24. Jiang Y, Purchase D, Jones H, Garelick H (2011) Effects of arsenate (AS5+) on growth and production of glutathione (GSH) and phytochelatins (PCS) in Chlorella vulgaris. Int. J. Phytoremediation 13:834–844CrossRefGoogle Scholar
  25. Jiang J, Qin C, Shu X, Chen R, Song H, Li Q, Xu H (2015) Effects of copper on induction of thiol-compounds and antioxidant enzymes by the fruiting body of Oudemansiella radicata. Ecotoxicol Environ Saf 111:60–65CrossRefGoogle Scholar
  26. Kim SB, Kim SH, Lee KR, Shim JO, Lee MW, Shim MJ, Lee UY, Lee TS (2005) The optimal culture conditions for the mycelial growth of Oudemansiella radicata. Mycobiology 33:230–234CrossRefGoogle Scholar
  27. Lan PY, Jian Z, Ping W, Jing Z, Rong T, Yu ZY, Zhi ML (2018) Effect of Cd on growth, physiological response, Cd subcellular distribution and chemical forms of Koelreuteria paniculata. Ecotoxicol Environ Saf 160:10–18CrossRefGoogle Scholar
  28. Li F, Fan Z, Xiao P, Oh K, Ma X, Hou W (2009) Contamination, chemical speciation and vertical distribution of heavy metals in soils of an old and large industrial zone in Northeast China. Environ Geol 57:1815–1823CrossRefGoogle Scholar
  29. Li H, Liu Y, Zeng G, Zhou L, Wang X, Wang Y, Wang C, Hu X, Xu W (2014) Enhanced efficiency of cadmium removal by Boehmeria nivea (L.) Gaud. in the presence of exogenous citric and oxalic acids. J Environ Sci 26:2508–2516CrossRefGoogle Scholar
  30. Li X, Dong S, Yuan Y, Shi W, Wu M, Xu H (2016) Inoculation of bacteria for the bioremediation of heavy metals contaminated soil by Agrocybe aegerita. RSC Adv 6:65816–65824CrossRefGoogle Scholar
  31. Li X, Wang Y, Pan Y, Yu H, Zhang X, Shen Y, Jiao S, Wu K, La G, Yuan Y (2017) Mechanisms of Cd and Cr removal and tolerance by macrofungus Pleurotus ostreatus HAU-2. J Hazard Mater 330:1–8CrossRefGoogle Scholar
  32. Liao M, Huang C (2002) Effects of organic acids on the toxicity of cadmium during ryegrass growth. Chin J Appl Ecol 13:109–112Google Scholar
  33. Lipka K, Falandysz J (2017) Accumulation of metallic elements by Amanita muscaria from rural lowland and industrial upland regions. J Environ Sci Health B 52:184–190CrossRefGoogle Scholar
  34. Liu H, Liu Y, Zeng G, Xie J, Zheng B, Tan X, Wang D, Sun Z, Nie J, Jiang Z (2015) Mitigation mechanism of Cd-contaminated soils by different levels of exogenous low-molecular-weight organic acids and Phytolacca americana. RSC Adv 5:47–49Google Scholar
  35. Lu L, Tian S, Zhang M, Zhang J, Yang X, Jiang H (2010) The role of Ca pathway in Cd uptake and translocation by the hyperaccumulator Sedum alfredii. J Hazard Mater 183:22–28CrossRefGoogle Scholar
  36. Luevano J, Damodaran C (2014) A review of molecular events of cadmium-induced carcinogenesis. J Environ Pathol Toxicol Oncol 33:183–194Google Scholar
  37. Ma L, Peng Y, Wu B, Lei D, Xu H (2013) Pleurotus ostreatus nanoparticles as a new nano-biosorbent for removal of Mn(II) from aqueous solution. Chem Eng J 225:59–67CrossRefGoogle Scholar
  38. Malar S, Vikram SS, Favas PJ, Perumal V (2016) Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)]. Bot Stud 55:1–11CrossRefGoogle Scholar
  39. Mihoub A, Bouhoun MD, Naeem A, Saker ML (2016) Low-molecular weight organic acids improve plant availability of phosphorus in different textured calcareous soils. Arch Agron Soil Sci 63:1023–1034CrossRefGoogle Scholar
  40. Mleczek M, Zuzanna M, Monika G, Przemysław N, Pavel K, Marek S, Piotr R, Sylwia Z, Krzysztof S (2016) Content of selected elements and low-molecular-weight organic acids in fruiting bodies of edible mushroom Boletus badius (Fr.) Fr. from unpolluted and polluted areas. Environ Sci Pollut Res 23:20609–20618CrossRefGoogle Scholar
  41. Montielrozas MM, Madejón E, Madejón P (2016) Effect of heavy metals and organic matter on root exudates (low molecular weight organic acids) of herbaceous species: an assessment in sand and soil conditions under different levels of contamination. Environ Pollut 216:273–281CrossRefGoogle Scholar
  42. Najeeb U, Jilani G, Ali S, Sarwar M, Xu L, Zhou W (2011) Insights into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid. J Hazard Mater 186:565–574CrossRefGoogle Scholar
  43. Rauser WE (1999) Structure and function of metal chelators produced by plants: the case for organic acids, amino acids, phytin, and metallothioneins. Cell Biochem Biophys 31:19–48CrossRefGoogle Scholar
  44. Sebastian A, Prasad MNV (2018) Exogenous citrate and malate alleviate cadmium stress in Oryza sativa L.: probing role of cadmium localization and iron nutrition. Ecotoxicol Environ Saf 166:215–222CrossRefGoogle Scholar
  45. Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321–336CrossRefGoogle Scholar
  46. Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307CrossRefGoogle Scholar
  47. Tica D, Udovic M, Lestan D (2011) Immobilization of potentially toxic metals using different soil amendments. Chemosphere 85:577–583CrossRefGoogle Scholar
  48. Tuzen M, Sesli E, Soylak M (2007) Trace element levels of mushroom species from East Black Sea region of Turkey. Food Control 18:806–810CrossRefGoogle Scholar
  49. Vig K, Megharaj M, Sethunathan N (2004) Bioavailability and toxicity of cadmium to microorganisms and their activities in soil: a review. Adv Environ Res 8:121–135CrossRefGoogle Scholar
  50. Wang SH, Shih YL, Ko WC, Wei YH, Shih CM (2008) Cadmium-induced autophagy and apoptosis are mediated by a calcium signaling pathway. Cell Mol Life Sci 65:3640–3652CrossRefGoogle Scholar
  51. Wu B, Cheng G, Kai J, Shi W, Wang C, Xu H (2016) Mycoextraction by Clitocybe maxima combined with metal immobilization by biochar and activated carbon in an aged soil. Sci Total Environ 562:732–739CrossRefGoogle Scholar
  52. Xiao K, Liu H, Dong S, Fan X, Chen Y, Xu H (2016) Interfacial effect of Stropharia rugoso-annulata in liquid medium: interaction of exudates and nickel-quintozene. RSC Adv 6:86068–86081CrossRefGoogle Scholar
  53. Xiao K, Li Y, Sun Y, Liu R, Li J, Zhao Y, Xu H (2017) Remediation performance and mechanism of heavy metals by a bottom-up activation and extraction system using multiple biochemical materials. ACS Appl Mater Interfaces 9:30448–30457CrossRefGoogle Scholar
  54. Xie H, Chen Y, Wang C, Shi W, Zuo L, Xu H (2015) The removal of fluoranthene by Agaricus bisporus immobilized in Ca-alginate modified by Lentinus edodes nanoparticles. RSC Adv 5:44812–44823CrossRefGoogle Scholar
  55. Xu H, Song P, Gu W, Yang Z (2011) Effects of heavy metals on production of thiol compounds and antioxidant enzymes in Agaricus bisporus. Ecotoxicol Environ Saf 74:1685–1692CrossRefGoogle Scholar
  56. Yang S, Sun X, Shen Y, Chang C, Guo E, La G, Zhao Y, Li X (2017) Tolerance and removal mechanisms of heavy metals by fungus Pleurotus ostreatus Haas. Water Air Soil Pollut 228:130–139CrossRefGoogle Scholar
  57. Zantua MI, Bremner JM (1975) Comparison of methods of assaying urease activity in soils. Soil Biol Biochem 7:291–295CrossRefGoogle Scholar
  58. Zhan F, Qin L, Guo X, Tan J, Liu N, Zu Y, Li Y (2016) Cadmium and lead accumulation and low-molecular-weight organic acids secreted by roots in an intercropping of a cadmium accumulator Sonchus asper L. with Vicia faba L. RSC Adv 6:33240–33248CrossRefGoogle Scholar
  59. Zhang W, Hu Y, Cao Y, Huang F, Xu H (2012) Tolerance of lead by the fruiting body of Oudemansiella radicata. Chemosphere 88:467–475CrossRefGoogle Scholar
  60. Zhang Q, Zhou W, Liang G, Sun J, Wang X, He P (2015) Distribution of soil nutrients, extracellular enzyme activities and microbial communities across particle-size fractions in a long-term fertilizer experiment. Appl Soil Ecol 94:59–71CrossRefGoogle Scholar
  61. Zhao F, Wang L, Gaohua JI, Weixing LI (2012) Effects of NaCl stress on plant biology indicators and MDA content of 3 submerged plants. Environ Pollut Control-in Chinese 34:40–44Google Scholar
  62. Zhuo S, Wang Y, Kang XF (2017) Engineered protein nanopore for real-time monitoring single-molecule reaction between cadmium ion and glutathione. Chin J Anal Chem 45:1172–1178CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life SciencesSichuan UniversityChengduPeople’s Republic of China
  2. 2.Institute of Soil and Groundwater Pollution Control of Sichuan Academy of Environmental SciencesChengduPeople’s Republic of China

Personalised recommendations