Skip to main content

Advertisement

Log in

Heavy metal bioaccumulation by wild edible saprophytic and ectomycorrhizal mushrooms

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Heavy metals cause serious problems in the environment, and they can be accumulated in organisms, especially in the higher fungi. The concentration of Ni, Cr, Pb, Cd, and Hg in 10 species of edible mushrooms in Medvednica Nature Park, Croatia was therefore determined. In addition, the similarity between the studied species was determined by cluster analysis based on concentrations of the aforementioned metals in the fruiting bodies. The contents of nickel, chromium, lead, cadmium, and mercury in the fruiting bodies of mushrooms were obtained by X-ray fluorescence spectrometry. The highest concentrations of Ni (3.62 mg kg−1), Cr (3.01 mg kg−1), and Cd (2.67 mg kg−1) were determined in Agaricus campestris. The highest concentration of Pb (1.67 mg kg−1) was determined in Macrolepiota procera, and the highest concentration of Hg (2.39 mg kg−1) was determined in Boletus edulis. The concentration of all heavy metals significantly differed (p < 0.001) between examined saprophytic and ectomycorrhizal mushrooms. Considering anatomical part of the fruiting body (cap-stipe), a considerably higher concentration of the analyzed elements was found in the cap for all mushroom species. According to calculated bioconcentration factors, all the examined species were found to be bioexclusors of Ni, Cr, and Pb and bioaccumulators of Cd and Hg. Cluster analysis performed on the basis of the accumulation of the studied metals revealed great phenotypic similarity of mushroom species belonging to the same genus and partial similarity of species of the same ecological affiliation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aloupi M, Koutrotsios G, Koulousaris M, Kalogeropoulos N (2012) Trace metal contents in wild edible mushrooms growing on serpentine and volcanic soils on the island of Levos, Greece. Ecotoxicol Environ Saf 78:184–194. doi:10.1016/j.ecoenv.2011.11.018

    Article  CAS  Google Scholar 

  • Amundson R, Richter DD, Humphreys GS, Jobbágy EG, Gaillardet J (2007) Coupling between biota and Earth materials in the critical zone. Elements 3:327–332. doi:10.2113/gselements.3.5.327

    Article  CAS  Google Scholar 

  • Baldrian P (2003) Interactions of heavy metals with white-rot fungi. Enzyme Mycrob Tech 32:78–91. doi:10.1016/S0141-0229(02)00245-4

    Article  CAS  Google Scholar 

  • Baldrian P (2008) Chapter 2: enzymes of saprotrophic basidiomycetes. In: Boddy L, Frankland JC, van West P (eds) Ecology of saprotrophic Basidiomycetes, vol 28, British Mycological Society Symposia Series. Elsevier, Amsterdam, pp 19–41

    Chapter  Google Scholar 

  • Baptista P, Ferreira S, Soares E, Coelho V, Bastos MD (2009) Tolerance and stress response of Macrolepiota procera nickel. J Agri Food Chem 57:7145–7152. doi:10.1021/jf902075b

    Article  CAS  Google Scholar 

  • Bellion M, Courbot M, Jacob C, Blaudez D, Chalot M (2006) Extracellular and cellular mechanisms sustaining metal tolerance in ectomycorrhizal fungi. FEMS Microbiol Lett 242:173–181

    Article  Google Scholar 

  • Blaudez D, Botton B, Chalot M (2000) Cadmium uptake and subcellular compartmentation in the ectomycorrhizal fungus Paxillus involutus. Mycrobiology 146:1109–1117. doi:10.1099/00221287-146-5-1109

    CAS  Google Scholar 

  • Bozac R (2005) Mushrooms encyclopaedia 1. Skolska knjiga, Zagreb pp. 598, ISBN 953-0-61413-6

  • Bozac R (2008) Mushrooms encyclopaedia 2. Skolska knjiga, Zagreb pp. 966, ISBN 978-953-0-61473-4

  • Brzostowski A, Falandysz J, Jarzynska G, Dan Z (2012) Bioconcentracion potential of metallic elements by Poison Pax (Paxillus involutus) mushroom. J Environ Sci Health Part A 46:378–393. doi:10.1080/10934529.2011.542387

    Article  Google Scholar 

  • Chojnacka A, Drewnowska M, Jarzynska G, Nnorom IC, Falandysz J (2012) Mercury in Yellow-cracking Boletes Xerocomus subtomentosus mushrooms and soils from spatially diverse sites: assessment of bioconcentration potential by species and human intake. J Environ Sci Health Part A 47:2094–2100. doi:10.1080/10934529.2012.695990

    Article  CAS  Google Scholar 

  • Chudzynski K, Falandysz J (2008) Multivariate analysis of elements content of Larch Bolete (Suillus gravillei). Chemosphere 73:1230–1239

    Article  CAS  Google Scholar 

  • Chudzynski K, Jarzynska G, Falandysz J (2013) Cadmium, lead and some other trace elements in Larch Bolete mushrooms (Suillus grevillei) (Klotzsch) Sing., collected from the same site over two years. Food Adit Contamin 6(4):249–253. doi:10.1080/19393210.2013.807881

    Article  CAS  Google Scholar 

  • Cocchi L, Vescovi L, Petrini LE, Petrini O (2006) Heavy metals in edible mushrooms in Italy. Food Chem 98:277–284. doi:10.1016/jfoodchem.2005.05.068

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Collin-Hansen C, Andersen RA, Steinnes E (2005b) Damage to DNA and lipids in Boletus edulis exposed to heavy metals. Mycolog Res 109:1386–1396

    Article  CAS  Google Scholar 

  • De Mendiburu F (2014) agricolae: statistical procedures for agricultural research. R package version 1.2-1. http://CRAN.R-project.org/package=agricolae

  • Demers JD, Driscoll CT, Fahey TJ, Yavitt JB (2007) Mercury cycling in litter and soil in different forest types in the Adirondack region, New York, USA. Ecol Appl 17:1341–1351

    Article  Google Scholar 

  • Drewnowska M, Falandysz J (2015) Investigtion on mineral composition and accumulation by popular edible mushroom common chanterelle (Cantharellus cibarius). Ecotox Env Saf 113:9–17. doi:10.1016/j.ecoenv.2014.11.028

    Article  CAS  Google Scholar 

  • Drewnowska M, Nnorom CI, Falandysz J (2014) Mercury in grisette. Amanita vaginata FR and soil below the fruiting bodies J Environ Sci Health Part B 49:521–526. doi:10.1080/03601234.2014.896677

    Article  CAS  Google Scholar 

  • Dryzalowskaa A, Falandysz J (2014) Bioconcentration of mercury by mushroom Xerocomus chrysenteron from the spatial distinct locations: levels, possible intake and safety. Ecotox Env Saf 107:97–102. doi:10.1016/j.ecoenv.2014.05.020

    Article  Google Scholar 

  • Falandysz J (2015) Mercury bio-extraction by fungus Coprinus comatus: a bioindicator and mycoremediator of polluted soils. Environ Sci Pollut Res 23(8):7444–741. doi:10.1007/s11356-015-5971-8

    Article  Google Scholar 

  • Falandysz J, Borovička R (2013) Macro and trace mineral constituents and radionuclides in mushrooms: health benefits and risks. Appl Microbiol Biotechnol 97:477–501. doi:10.1007/s00253-012-4552-8

    Article  CAS  Google Scholar 

  • Falandysz J, Gucia M, Mazur A (2007) Content and biconcentration factors of mercury by Parasol Mushrooms Macrolepiota procera. J Environ Sci Health Part B 42:735–740

    Article  CAS  Google Scholar 

  • Falandysz J, Szymczyk K, Ichihashi H, Bielawski L, Gucia M, Frankowska A, Yamasaki SI (2001) ICP/MS and ICP/AES elemental analysis (38 elements) of edible wild mushrooms growing in Poland. Food Addit Contam 18:503–513

    Article  CAS  Google Scholar 

  • Falandysz J, Mazur A, Kojta AK, Jarzynska G, Drewnowska M, Dryzalowska A, Nnorom IC (2012) Mercury in fruiting bodies of dark honey fungus (Armillaria solidipes) and beneath substratum soils collected from spatially distant areas. J Sci Food Agric 93:853–858. doi:10.1002/jsfa.5807

    Article  Google Scholar 

  • Falandysz J (2014) Distribution of mercury in Gypsy Cortinarius caperatus mushrooms from several populations: an efficient accumulator species and estimated intake of element. Ecotox Environ Safe 110:68–72. doi:10.1016/j.ecoenv.2014.08.018

    Article  CAS  Google Scholar 

  • Falandysz J, Krasinska G, Pankavec S, Nnorom CI (2014) Mercury in certain boletus mushrooms from Poland and Belarus. J Environ Sci Health Part B 49:690–695. doi:10.1080/03601234.2014.922853

    Article  CAS  Google Scholar 

  • Falandysz J, Zhang J, Wang Y, Krasinska G, Kojta A, Saba M, Shen T, Li T, Liu H (2015a) Evaluation of mercury contamination in mushrooms of genus Leccinum from two different rgions of the world: accumulation, distribution and probalbe dietary intake. Sci Total Environ 537:470–478. doi:10.1016/j.scitotenv.2015.07.159

    Article  CAS  Google Scholar 

  • Falandysz J, Zhang J, Wang YZ, Saba M, Krasinska G, Wiejak A, Li T (2015b) 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. PlosOne, 1–19. doi: 10.371/journal.pone.0143608.

  • Falandysz J, Drewnowska M (2015) Macro and trace elements in common chanterelle (Cantharellus cibarius) mushroom from the European background areas in Poland: composition, accumulation, dietary exposure and data review for species. J Environ Sci Health Part B 50:374–387. doi:10.1080/03601234.2015.1000190

    Article  CAS  Google Scholar 

  • Figueiredo E, Soares ME, Baptista P, Castro M, Bastos ML (2007) Validation of an electrothermal atomatization absorption spectrometry method for quantification of total chromium and chromium IV in wild edible mushrooms and underlying soils. J Agric Food Chem 55:7192–7198

    Article  CAS  Google Scholar 

  • García MÁ, Alonso J, Melgar MJ (2009) Lead in edible mushrooms. Levels and bioaccumulation factors J Hazard Mater 167:777–783. doi:10.1016/j.jhazmat.2009.01.058

    Article  Google Scholar 

  • 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. doi:10.1016/j.fct.2013.04.049

    Article  CAS  Google Scholar 

  • Gucia M, Jarzynska G, Kojta A, Falandysz J (2012a) Temporal variability in 20 chemical elements content of Parasol Mushroom (Macrolepiota procera) collected from two sites over a few years. J Environ Sci Health Part B 47:81–88. doi:10.1080/03601234.2012.611433

    Article  CAS  Google Scholar 

  • Gucia M, Jarzynska G, Rafal E, Roszak M, Kojta AK, Osiej I, Falandysz J (2012b) Multivariate analysis of mineral constituents of edible Parasol Mushroom (Macrolepiota procera) and soils beneath fruiting bodies collected from Northern Poland. Environ Sci Pollut Res 19:416–431. doi:10.1007/s11356-011-0574-5

    Article  CAS  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50(3):346–363

    Article  Google Scholar 

  • Işıldak Ö, Turkekul I, Elmastas M, Aboul-Enein HY (2007) Bioaccumulation of heavy metals in some wild-grown edible mushrooms. Anal Lett 40:1099–1116. doi:10.1080/00032710701297042

    Article  Google Scholar 

  • Işıldak Ö, Turkekul I, Elmastas M, Tüzen M (2004) Analysis of heavy metals in some wild-grown edible mushrooms from the middle Black Sea region, Turkey. Food Chem 86:547–552. doi:10.1016/j.foodchem.2003.09.007

    Article  Google Scholar 

  • Jarzynska G, Falandysz J (2012) Metallic elements profile of Hazel (Hard) Bolete (Leccinum griseum) mushroom and associated upper soil horizon. Afr J Biotechnol 11:4588–4594

    CAS  Google Scholar 

  • Jarzynska G, Gucia M, Kojta A, Rezulak K, Falandysz J (2011) Profile of trace elements in Parasol Mushroom (Macrolepiota procera) from Tucholskie Forest. J Environ Sci Halth Part B 46:741–751. doi:10.1080/03601234.2011.603986

    CAS  Google Scholar 

  • Jennings DH (2007) The physiology of fungal nutrition. Cambridge University Press, pp 460. ISBN: 9780521038164

  • Jorhem L, Sundstrom B (1995) Levels of some trace elements in edible fungi. Z Lebensm Unters Forsch 201:311–316

    Article  CAS  Google Scholar 

  • Kalač P (2001) A review of edible mushroom radioactivity. Food Chem 75:29–35. doi:10.1016/S0308-8146(01)00171-6

    Article  Google Scholar 

  • Kalač P, Svoboda L (2000) A review of trace elements concentrations in edible mushrooms. Food Chem 69:273–281. doi:10.1016/S0308-8146(99)00264-2

    Article  Google Scholar 

  • 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. doi:10.1016/j.foodchem.2010.02.045

    Article  Google Scholar 

  • Kojta AK, Gucia M, Jarzynska G, Lewandowska M, Zakrzewska A, Falandysz J, Zhang D (2011) Phosphorus and certain metals in parasol mushrooms (Macrolepiota procera) and soils from the Augustowska forest and Elk region in north-eastern Poland. Fresenius Environ Bull 20:3044–3052

    CAS  Google Scholar 

  • Krasinska G, Falandysz J (2015) Mercury in Hazel Bolete Leccinum griseum and soil substratum: distribution, bioconcentration and dietary exposure. J Environ Sci Halth Part A 50:1259–1264. doi:10.1080/10934529.2015.1055151

    Article  CAS  Google Scholar 

  • Krasinska G, Falandysz J (2016) Mercury in Orange Birch Bolete Leccinum versipelle and soil substratum: bioconcentration by mushroom and probable dietary intake by consumers. Environ Sci Pollut Res 53:86–869. doi:10.1007/s11356-015-5331-8

    Google Scholar 

  • Kuldo E, Jarzynska G, Gucia M, Falandysz J (2014) Mineral constituents of edible parasol mushroom Macrolepiota procera (Scop. ex Fr.) Sing and soils beneath its fruiting bodies collected from a rural forest area. Chem Pap 68(4):484–492. doi:10.2478/s11696-013-0477-7

    Article  CAS  Google Scholar 

  • 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. doi:10.1016/j.foodchem.2011.02.012

    Article  CAS  Google Scholar 

  • Malinowska E, Szefer P, Falandysz J (2004) Metals bioaccumulation by bay bolete, Xerocomus badius, from selected sites in Poland. Food Chem 84:405–416. doi:10.1016/S0308-8146(03)00250-4

    Article  CAS  Google Scholar 

  • Manzi P, Aguzzi A, Vivanti V, Paci M, Pizzoferrato L (1999) Mushrooms as a source of functional ingredients. In Euro. Food Chem X European conference on functional foods. A new challenge for the food chemist 1: 86–93, 22–24 September, Budapest, Hungary

  • Melgar MJ, Alonso J, Garcia MA (2009) Mercury in edible mushrooms and underlying soil: bioconcentration factor and toxicological risks. Sci Total Environ 407:2328–2334. doi:10.1016/j.scitotenv.2009.07.001

    Article  Google Scholar 

  • Mendil D, Ulüozlü ÖD, Tüzen M, Hasdemir E, Çaglar A (2004) Determination of trace elements on some wild edible mushroom samples from Kastamonu, Turkey. Food Chem 88:281–285. doi:10.1016/j.foodchem.2004.01.039

    Article  CAS  Google Scholar 

  • Nikkarinen M, Mertanen E (2004) Impact of geological origin on trace element composition of edible mushrooms. J Food Compos Anal 17:301–310. doi:10.1016/j.jfca.2004.03.013

    Article  CAS  Google Scholar 

  • Official Gazette 154/08 (2008). Regulations on maximum levels of certain contaminants in foodstuffs. National Journal, Zagreb, Croatia

  • Ouzouni PK, Petridis D, Koller WD, Kyriakos A, Riganakos KA (2009) Nutritional value and metal content of wild edible mushrooms collected from West Macedonia and Epirus, Greece. Food Chem 115:1575–1580. doi:10.1016/j.foodchem.2009.02.014

    Article  CAS  Google Scholar 

  • Ouzuni PK, Veltsistas PG, Paleologos EK, Riganakos KA (2007) Determination of metal content in wild edible mushroom species from regions of Greece. J Food Compos Anal 20:480–486. doi:10.1016/j.jfca.2007.02.008

    Article  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetic and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  Google Scholar 

  • Pelkonen R, Alfthan G, Järvinen O (2006) Cadmium, lead, arsenic and nickel in wild edible mushrooms. The Finnish Environment 17/2006

  • Petkovšek SS, Pokorny B (2013) Lead and cadmium in mushrooms from the vicinity of two large emission sources in Slovenia. Sci Total Environ 443:944–954. doi:10.1016/j.scitotenv.2012.11.007

    Article  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/

  • Saba M, Falandysz J, Nnorom IC (2016) Accumulation and distribution of mercury in fruiting bodies by fungus Suillus luteus forged in Poland, Belarus and Sweden. Environ Sci Pollut Res 23:2749–2757. doi:10.1007/s11356-015-5513-4

    Article  CAS  Google Scholar 

  • Sarkar D (2008) Lattice: multivariate data visualization with R. Springer, New York. ISBN 978-0-387-75968-5

  • Sarikurkcu C, Copur M, Yildiz D, Akata I (2011) Metal concentration of wild edible mushrooms in Soguksu National Park in Turkey. Food Chem 128:731–734. doi:10.1016/j.foodchem.2011.03.097

    Article  CAS  Google Scholar 

  • Schuster PF, Krabbenhoft DP, Naftz DL, Cecil LD, Olson ML, Dewild JF, Susong DD, Green JR, Abbott ML (2002) Atmospheric mercury deposition during the last 270 years: a glacial ice core record of natural and anthropogenic sources. Environ Sci Technol 36:2303–2310

    Article  CAS  Google Scholar 

  • Smith ML, Bruhn JN, Anderson JB (1992) The fungus Armillaria bulbosa is among the largest and oldest living organisms. Nature 356:428–431. doi:10.1038/356428a0

    Article  Google Scholar 

  • Soylak M, Saracoglu S, Tüzen M, Mendil D (2005) Determination of trace metals in mushroom samples from Kayseri, Turkey. Food Chem 92:649–652. doi:10.1016/j.foodchem.2004.08.032

    Article  CAS  Google Scholar 

  • Stefanović V, Trifković J, Mutić J, Tešić Ž (2016) Metal accumulation capacity of parasol mushroom (Macrolepiota procera) from Rasina region (Serbia). Environ Sci Pollut Res 1–13. doi:10.1007/s11356-016-6486-7

  • Svoboda L, Havlickova B, Kalač P (2006) Contents of cadmium, mercury and lead in edible mushrooms growing in a historical silver-mining area. Food Chem 96:580–585. doi:10.1016/j.foodchem.2005.03.012

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Širić I, Kos I, Bedeković D, Kaić A, Kasap A (2014) Heavy metals in edible mushrooms Boletus reticulatus Schaeff. collected from Zrin, mountain, Croatia. Period Boil 116:319–322

    Google Scholar 

  • Thomas GW (1996) Soil pH and soil acidity. Methods of soil analysis. Part 3—chemical methods. Soil Science Society of America and American Society of Agronomy 5:457–490

  • Thomet U, Vogel E, Krahenbuhl U (1999) The uptake of cadmium and zinc by mycelia and their accumulation in fruiting bodies of edible mushrooms. Eur Food Res Technol 209:317–324

    Article  CAS  Google Scholar 

  • Turkdogan KM, Kilicel F, Kara K, Tuncer I, Uygan I (2003) Heavy metals in soil, vegetables and fruits in the endemic upper gastrointestinal cancer region of Turkey. Environ Toxicol Pharmacol 13:175–179. doi:10.1016/S1382-6689(02)00156-4

    Article  CAS  Google Scholar 

  • Turkekul I, Elmastas M, Tuzen M (2004) Determination of iron, copper, manganese, zinc, leads and cadmium in mushrooms samples from Tokat, Turkey. Food Chem 84:389–392. doi:10.1016/S0308-8146(03)00245-0

    Article  CAS  Google Scholar 

  • UNEP, 2013. Mercury—time to act. United Nations Environmental Programme (http://www.unep.org/PDF/PressReleases/Mercury_TimeToAct.pdf)

  • van Schöll L, Hoffland E, van Breemen N (2006) Organic anion exudation by ectomycorrhizal fungi and Pinus sylvestris in response to nutrient deficiencies. New Phytol 170:153–163. doi:10.1111/j.1469-8137.2006.01649.x

    Article  Google Scholar 

  • Vetter J (2004) Arsenic content of some edible mushroom species. Eur Food Res Technol 219:71–74

    Article  CAS  Google Scholar 

  • Wang Z, Chen J, Chai L, Yang Z, Huang S, Zheng Y (2011) Environmental impact and site-specific human health risks of chromium in the vicinity of a ferro-alloy manufactory, China. J Hazard Mater 190:80–985

    Google Scholar 

  • Yamaç M, Yildiz D, Sarikurcu C, Celikkollu M, Solak MH (2007) Heavy metals in some edible mushrooms from the Central Anatolia, Turkey. Food Chem 103:263–267. doi:10.1016/j.foodchem.2006.07.041

    Article  Google Scholar 

  • Żarski TP, Żarska H, Arkuszewska E, Válka J, Sokol J, Beseda I (1999) The bioindicative role of mushrooms in the evaluation of environmental contamination with mercury compounds. Ekol Bratislava 18:223–229

    Google Scholar 

Download references

Acknowledgments

The authors would like to thank Professor Romano Božac for help, organization, and support during the collection and identification of mushrooms.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Miha Humar.

Additional information

Responsible editor: Elena Maestri

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Širić, I., Humar, M., Kasap, A. et al. Heavy metal bioaccumulation by wild edible saprophytic and ectomycorrhizal mushrooms. Environ Sci Pollut Res 23, 18239–18252 (2016). https://doi.org/10.1007/s11356-016-7027-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-7027-0

Keywords

Navigation