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Contents and Health Risk Assessment of Elements in Three Edible Ectomycorrhizal Fungi (Boletaceae) from Polymetallic Soils in Yunnan Province, SW China

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Abstract

Ectomycorrhizal fungi (EcMF) can mobilize mineral elements directly from insoluble mineral sources and accumulate various metallic elements and metalloids from soils to their fruiting bodies. Mushrooms from genus Boletus and its related genus are one of the most important EcMF which are consumed worldwide as wild edible mushrooms. Yunnan province (China) is a high biodiversity of genus Boletus mushrooms but is also an area with potential elevated contents of toxic elements in soil. Total contents of As, Ag, Ba, Cd, Co, Cr, Cs, Cu, Li, Mn, Ni, Pb, Rb, Sb, Sr, Tl, U, V, and Zn in three edible EcMF species collected from five sites of Yunnan were analyzed by inductively coupled plasma mass spectrometer. The highest contents for As, Cd, and Pb were 7.8 mg kg−1 dry weight (dw) in the caps of Butyriboletus roseoflavus, 3.4 mg kg−1 dw in the caps of B. roseoflavus, and 6.4 mg kg−1 dw in the stipes of Hemileccinum impolitum. Health risk assessment of As, Cd, and Pb indicated that the estimated exposure due to intakes of some mushroom samples from the sites were above the limits recommended by the Joint FAO/WHO Expert Committee on Food Additives. Since EcMF were considered as bioexclusors of Cr, higher Cr contents in the mushroom samples, compared with previous studies, indicated high geochemical background value of Cr in the sampling sites. Relatively higher V contents in mushrooms from family Boletaceae could also associate with the high V contents in Yunnan soil. Further work is needed to identify the places in Yunnan with geochemical anomalies resulting in high levels of toxic elements in EcMF.

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References

  1. Taylor LL, Leake JR, Quirk J, Hardy K, Banwart SA, Beerling DJ (2009) Biological weathering and the long-term carbon cycle: integrating mycorrhizal evolution and function into the current paradigm. Geobiology 7:171–191

    CAS  PubMed  Google Scholar 

  2. Landeweert R, Hoffland E, Finlay RD, Kuyper TW, van Breemen N (2001) Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends Ecol Evol 16:248–254

    CAS  PubMed  Google Scholar 

  3. Falandysz J, Borovička J (2013) Macro and trace mineral constituents and radionuclides in mushrooms: health benefits and risks. Appl Microbiol Biotechnol 97:477–501

    CAS  PubMed  Google Scholar 

  4. Jing XB, He N, Zhang Y, Cao YR, Xu H (2011) Isolation and characterization of heavy-metal-mobilizing bacteria from contaminated soils and their potential in promoting Pb, Cu, and Cd accumulation by Coprinus comatus. Can J Microbiol 58:45–53

    PubMed  Google Scholar 

  5. Lepšová A, Mejstřík V (1988) Accumulation of trace elements in the fruiting bodies of macrofungi in the Krušné hory mountains, Czechoslovakia. Sci Total Environ 76:117–128

    PubMed  Google Scholar 

  6. Cui YY, Feng B, Wu G, Xu J, Yang ZL (2016) Porcini mushrooms (Boletus sect. Boletus) from China. Fungal Divers 81:189–212

    Google Scholar 

  7. Borovička J, Dunn CE, Gryndler M, Mihaljevič M, Jelínek E, Rohovec J, Rohošková M, Řanda Z (2010a) Bioaccumulation of gold in macrofungi and ectomycorrhizae from the vicinity of the Mokrsko gold deposit, Czech Republic. Soil Biol Biochem 42:83–91

    Google Scholar 

  8. Borovička J, Kotrba P, Gryndler M, Mihaljevič M, Řanda Z, Rohovec J, Cajthaml T, Stijve T, Dunn CE (2010b) Bioaccumulation of silver in ectomycorrhizal and saprobic macrofungi from pristine and polluted areas. Sci Total Environ 408:2733–2744

    PubMed  Google Scholar 

  9. Falandysz J, Rizal LM (2016) Arsenic and its compounds in mushrooms: a review. J Environ Sci Health C 34:217–232

    CAS  Google Scholar 

  10. Mleczek M, Niedzielski P, Siwulski M, Rzymski P, Gąsecka M, Goliński P, Kozak L, Kozubik T (2016b) Importance of low substrate arsenic content in mushroom cultivation and safety of final food product. Eur Food Res Technol 242:355–362

    CAS  Google Scholar 

  11. Mleczek M, Niedzielski P, Rzymski P, Siwulski M, Gąsecka M, Kozak L (2016a) Variations of arsenic species content in edible Boletus badius growing at polluted sites over four years. J Environ Sci Health B 51:469–476

    CAS  PubMed  Google Scholar 

  12. Liu B, Huang Q, Cai H, Guo X, Wang T, Gui M (2015) Study of heavy metal concentrations in wild edible mushrooms in Yunnan Province, China. Food Chem 188:294–300

    CAS  PubMed  Google Scholar 

  13. Liu Y, Chen D, You Y, Zeng S, Li Y, Tang Q, Han G, Liu A, Feng C, Li C, Su Y, Su Z, Chen D (2016) Nutritional composition of Boletus mushrooms from Southwest China and their antihyperglycemic and antioxidant activities. Food Chem 211:83–91

    CAS  PubMed  Google Scholar 

  14. Kalač P (2010) Trace element contents in European species of wild growing edible mushrooms: a review for the period 2000–2009. Food Chem 122:2–15

    Google Scholar 

  15. Flora G, Gupta D, Tiwari A (2012) Toxicity of lead: a review with recent updates. Interdiscip Toxicol 5:47–58

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Garcia MA, Alonso J, Fernández MI, Melgar MJ (1998) Lead content in edible wild mushrooms in northwest Spain as indicator of environmental contamination. Arch Environ Contam Toxicol 34:330–335

    CAS  PubMed  Google Scholar 

  17. Wu G, Li YC, Zhu XT, Zhao K, Han LH, Cui YY, Li F, Xu JP, Yang ZL (2016) One hundred noteworthy boletes from China. Fungal Divers 81:25–188

    Google Scholar 

  18. Falandysz J, Zhang J, Wang YZ, Saba M, Krasińska G, Wiejak A, Li T (2015) Evaluation of mercury contamination in fungi boletus species from latosols, lateritic red earths, and red and yellow earths in the circum-Pacific mercuriferous belt of southwestern China. PLoS One 10:e0143608

    PubMed  PubMed Central  Google Scholar 

  19. Weng H, Liu Y, Chen H (1997) Environmental geochemical features of arsenic in soil in China. J Environ Sci 9:385–395

    Google Scholar 

  20. Yang J, Teng Y, Wu J, Chen H, Wang G, Song L, Yue W, Zuo R, Zhai Y (2017) Current status and associated human health risk of vanadium in soil in China. Chemosphere 171:635–643

    CAS  PubMed  Google Scholar 

  21. Gao Y, Xia J (2011) Chromium contamination accident in China: viewing environment policy of China. Environ Sci Technol 45:8605–8606

    CAS  PubMed  Google Scholar 

  22. Wang XM, Zhang J, Li T, Li JQ, Wang YZ, Liu HG (2015) ICP-AES determination of mineral content in Boletus tomentipes collected from different sites of China. Spectrosc Spectr Anal 35:1398–1403

    CAS  Google Scholar 

  23. Wang XM, Zhang J, Li T, Li JQ, Wang YZ, Liu HG (2015) Variations in element levels accumulated in different parts of Boletus edulis collected from Central Yunnan Province, China. J Chem 2015:372152

    Google Scholar 

  24. Wang XM, Liu HG, Zhang J, Li T, Wang YZ (2017) Evaluation of heavy metal concentrations of edible wild-grown mushrooms from China. J Environ Sci Heal B 52:178–183

    CAS  Google Scholar 

  25. Mao XL (2000) The macrofungi of China. Henan Science and Technology Press, Zhengzhou

    Google Scholar 

  26. Wang XH, Liu PG, Yu FQ (2004) Color atlas of wild commercial mushrooms in Yunnan. Yunnan Science and Technology Press, Kunming

    Google Scholar 

  27. Mędyk M, Chudzińska M, Barałkiewicz D, Falandysz J (2017) Specific accumulation of cadmium and other trace elements in Sarcodon imbricatus using ICP-MS with a chemometric approach. J Environ Sci Health B 52:361–366

    PubMed  Google Scholar 

  28. Falandysz J, Chudzińska M, Barałkiewicz D, Saba M, Wang Y, Zhang J (2017) Occurrence, variability and associations of trace metallic elements and arsenic in sclerotia of medicinal Wolfiporia extensa from polymetallic soils in Yunnan, China. Acta Poloniae Pharmaceutica, Drug Res 74:1379–1387

    CAS  Google Scholar 

  29. Falandysz J, Zhang J, Wiejak A, Barałkiewicz D, Hanć A (2017b) Metallic elements and metalloids in Boletus luridus, B. magnificus and B. tomentipes mushrooms from polymetallic soils from SW China. Ecotox Environ Safe 142:497–502

    CAS  Google Scholar 

  30. JECFA (2010a) Joint FAO/WHO Expert Committee on Food Additives seventy-second meeting Rome, 16–25 February 2010, Food and Agriculture Organization of the United Nations World Health Organization

  31. JECFA (2010b) Joint FAO/WHO eExpert Committee on Food Additives seventy-third meeting Geneva, 8–17 June 2010 Food and Agriculture Organization of the United Nations World Health Organization

  32. Li T, Wang Y, Zhang J, Zhao Y, Liu H (2011) Trace element content of Boletus tomentipes mushroom collected from Yunnan, China. Food Chem 127:1828–1830

    CAS  Google Scholar 

  33. Zhang J, Liu H, Li SJ, Li JQ, Wang Y, Li T (2015) Arsenic in edible and medicinal mushrooms from Southwest China. Int J Med Mushrooms 17:601–605

    PubMed  Google Scholar 

  34. Xing B, Zhang J, Li J, Wang Y, Liu H (2016) Determination of mineral elements contents in eight wild Boletus species from Yunnan by ICP-MS. Food Sci 37:89–94 (in Chinese with English abstract)

    Google Scholar 

  35. Yang TW, Zhang J, Liu HG, Wang YZ (2016) Determination and food safety assessment of arsenic in wild-grown bolete mushrooms from Yunnan province. Asian J Ecotoxicol 11:755–761 (in Chinese with English abstract)

    Google Scholar 

  36. Zheng GQ, Wang L, Li J (2014) Assessment of lead, arsenic, and mercury in wild-grown mushrooms from Baoshan, Yunnan. Strait J Prev Med 20:58–59 (in Chinese)

    Google Scholar 

  37. Cocchi L, Vescovi L, Petrini LE, Petrini O (2006) Heavy metals in edible mushrooms in Italy. Food Chem 98:277–284

    CAS  Google Scholar 

  38. Dimitrijevic MV, Mitic VD, Cvetkovic JS, Jovanovic VPS, Mutic JJ, Mandic SDN (2016) Update on element content profiles in eleven wild edible mushrooms from family Boletaceae. Eur Food Res Technol 242:1–10

    CAS  Google Scholar 

  39. Xiao XY, Chen TB, Liao XY, Wu B, Yan XL, Zhai LM, Xie H, Wang LX (2008) Regional distribution of arsenic contained minerals and arsenic pollution in China. Geogr Res 27:201–212

    Google Scholar 

  40. Chen S, Guo Q, Liu L (2017) Determination of arsenic species in edible mushrooms by high-performance liquid chromatography coupled to inductively coupled plasma mass spectrometry. Food Anal Methods 10:740–748

    Google Scholar 

  41. Komorowicz I, Hanć A, Lorenc W, Barałkiewicz D, Falandysz J, Wang Y (2019) Arsenic speciation in mushrooms using dimensional chromatography coupled to ICP-MS detector. Chemosphere 233:223–233

    CAS  PubMed  Google Scholar 

  42. Braeuer S, Goessler W, Kameník J, Konvalinková T, Žigová A, Borovička J (2018) Arsenic hyperaccumulation and speciation in the edible ink stain bolete (Cyanoboletus pulverulentus). Food Chem 242:225–231

    CAS  PubMed  Google Scholar 

  43. Kenyon EM, Hughes MF (2001) A concise review of the toxicity and carcinogenicity of dimethylarsinic acid. Toxicology 160:227–236

    CAS  PubMed  Google Scholar 

  44. Ma P, Zhang D, Yang LB, Zeng XD (2012) Bioaccumulation of heavy metal in wild edible Boletus fruiting body. Environ Sci Technol 35:5–8 (in Chinese with English abstract)

    CAS  Google Scholar 

  45. Zhao B (2007) Study on the safety evaluation and control methods of four species of Boletus. Master’s Degree Thesis. Southwest University, Chongqing. (in Chinese with English abstract)

  46. Blanuša M, Kučak A, Varnai VM, Sarić MM (2001) Uptake of cadmium, copper, iron, manganese, and zinc in mushrooms (Boletaceae) from Croatian forest soil. J AOAC Int 84:1964–1971

    PubMed  Google Scholar 

  47. Vetter J (1994) Data on arsenic and cadmium contents of some common mushrooms. Toxicon 32:11–15

    CAS  PubMed  Google Scholar 

  48. Širić I, Kasap A, Bedeković D, Falandysz J (2017) Lead, cadmium and mercury contents and bioaccumulation potential of wild edible saprophytic and ectomycorrhizal mushrooms, Croatia. J Environ Sci Health B 52:156–165

    PubMed  Google Scholar 

  49. Falandysz J, Kunito T, Kubota R, Bielawski L, Frankowska A, Falandysz JJ, Tanabe S (2008) Multivariate characterization of elements accumulated in King Bolete Boletus edulis mushroom at lowland and high mountain regions. J Environ Sci Health A 43:1692–1699

    CAS  Google Scholar 

  50. Collin-Hansen C, Andersen RA, Steinnes E (2005) Molecular defense systems are expressed in the king bolete (Boletus edulis) growing near metal smelters. Mycologia 97:973–983

    CAS  PubMed  Google Scholar 

  51. Borovička J, Kubrová J, Rohovec J, Řanda Z, Dunn CE (2011) Uranium, thorium and rare earth elements in macrofungi: what are the genuine concentrations? Biometals 24:837–845

    PubMed  Google Scholar 

  52. García MÁ, Alonso J, Melgar MJ (2009) Lead in edible mushrooms: levels and bioaccumulation factors. J Hazard Mater 167:777–783

    PubMed  Google Scholar 

  53. Cejpková J, Gryndler M, Hršelová H, Kotrba P, Řanda Z, Synková I, Borovička J (2016) Bioaccumulation of heavy metals, metalloids, and chlorine in ectomycorrhizae from smelter-polluted area. Environ Pollut 218:176–185

    PubMed  Google Scholar 

  54. Byrne AR, Dermelj M, Vakselj T (1979) Silver accumulation by fungi. Chemosphere 8:815–821

    CAS  Google Scholar 

  55. Falandysz J, Bona H, Danisiewicz D (1994) Silver content of wild-grown mushrooms from Northern Poland. Z Lebensm Unters Forsch 199:222–224

    CAS  PubMed  Google Scholar 

  56. Falandysz J, Frankowska A, Jarzyńska G, Dryżałowska A, Kojta AK, Zhang D (2011) Survey on composition and bioconcentration potential of 12 metallic elements in King Bolete (Boletus edulis) mushroom that emerged at 11 spatially distant sites. J Environ Sci Health B 46:231–246

    CAS  PubMed  Google Scholar 

  57. Frankowska A, Ziółkowska J, Bielawski L, Falandysz J (2010) Profile and bioconcentration of minerals by King Bolete (Boletus edulis) from the Płocka Dale in Poland. Food Addit Contam B 3:1–6

    CAS  Google Scholar 

  58. Zhang D, Frankowska A, Jarzyńska G, Kojta AK, Drewnowska M, Wydmańska D, Bielawski L, Wang J, Falandysz J (2010) Metals of King Bolete (Boletus edulis) Bull.: Fr. collected at the same site over two years. Afr J Agric Res 5:3050–3055

    Google Scholar 

  59. Liu H, Zhang J, Li T, Shi Y, Wang Y (2012) Mineral element levels in wild edible mushrooms from Yunnan, China. Biol Trace Elem Res 147:341–345

    CAS  PubMed  Google Scholar 

  60. Borovička J, Řanda Z (2007) Distribution of iron, cobalt, zinc and selenium in macrofungi. Mycol Prog 6:249–259

    Google Scholar 

  61. Garcia MA, Alonso J, Melgar MJ (2013) Bioconcentration of chromium in edible mushrooms: influence of environmental and genetic factors. Food Chem Toxicol 58:249–254

    CAS  PubMed  Google Scholar 

  62. Svoboda L, Zimmermannová K, Kalač P (2000) Concentrations of mercury, cadmium, lead and copper in fruiting bodies of edible mushrooms in an emission area of a copper smelter and a mercury smelter. Sci Total Environ 246:61–67

    CAS  PubMed  Google Scholar 

  63. Vetter J (2005) Lithium content of some common edible wild-growing mushrooms. Food Chem 90:31–37

    CAS  Google Scholar 

  64. Kojta AK, Falandysz J (2016) Metallic elements (Ca, Hg, Fe, K, Mg, Mn, Na, Zn) in the fruiting bodies of Boletus badius. Food Chem 200:206–214

    CAS  PubMed  Google Scholar 

  65. Wang XM, Zhang J, Li T, Wang YZ, Liu HG (2015c) Content and bioaccumulation of nine mineral elements in ten mushroom species of the genus Boletus. J Anal Methods Chem 2015:165412

    PubMed  PubMed Central  Google Scholar 

  66. Reczyński W, Muszyńska B, Opoka W, Smalec A, Sułkowska-Ziaja K, Malec M (2013) Comparative study of metals accumulation in cultured in vitro mycelium and naturally grown fruiting bodies of Boletus badius and Cantharellus cibarius. Biol Trace Elem Res 153:355–362

    PubMed  PubMed Central  Google Scholar 

  67. Kalač P (2013) A review of chemical composition and nutritional value of wild-growing and cultivated mushrooms. J Sci Food Agric 93:209–218

    PubMed  Google Scholar 

  68. Borovička J, Řanda Z, Jelínek E (2006) Antimony content of macrofungi from clean and polluted areas. Chemosphere 64:1837–1844

    PubMed  Google Scholar 

  69. Širić I, Žurga P, Barkić D, Malenica Staver M (2016) Trace element contents in the edible mushroom Boletus edulis Bull. ex Fries. Agric Conspec Sci 80:223–227

    Google Scholar 

  70. Svoboda L, Chrastný V (2008) Levels of eight trace elements in edible mushrooms from a rural area. Food Addit Contam 25:51–58

    CAS  Google Scholar 

  71. Gadd GM, Fomina M (2011) Uranium and fungi. Geomicrobiol J 28:471–482

    CAS  Google Scholar 

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Funding

This work was financially supported by the National Natural Science Foundation of China (grant number 31660591).

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Authors and Affiliations

  1. Institute of Medicinal Plants, Yunnan Academy of Agricultural Sciences, Kunming, 650200, China

    Ji Zhang, Jerzy Falandysz & Yuanzhong Wang

  2. Key Laboratory of Tropical Plant Resources and Sustainable Use, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, 666303, China

    Ji Zhang

  3. Department of Trace Element Analysis by Spectroscopy Method, Adam Mickiewicz University, 61-614, Poznań, Poland

    Danuta Barałkiewicz & Anetta Hanć

  4. Environmental Chemistry & Ecotoxicology, University of Gdańsk, 80-309, Gdańsk, Poland

    Jerzy Falandysz

  5. Environmental and Computational Chemistry Group, University of Cartagena, Cartagena, 130015, Colombia

    Jerzy Falandysz

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  1. Ji Zhang
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  2. Danuta Barałkiewicz
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  4. Jerzy Falandysz
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Correspondence to Ji Zhang.

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Zhang, J., Barałkiewicz, D., Hanć, A. et al. Contents and Health Risk Assessment of Elements in Three Edible Ectomycorrhizal Fungi (Boletaceae) from Polymetallic Soils in Yunnan Province, SW China. Biol Trace Elem Res 195, 250–259 (2020). https://doi.org/10.1007/s12011-019-01843-y

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