Wild-growing mushrooms (macromycetes, macrofungi) are capable of accumulating high amounts of trace elements, including noble metals. In a series of analytical experiments, this study focused on the problem of correct determination of Ag mass fractions in the biomass of Ag-accumulating mushrooms, Ag-hyperaccumulators in particular. A unique experimental setup enabled to compare Ag determination in selected mushroom samples first by the non-destructive neutron activation analysis (INAA) utilizing 110Ag isotope, second by the high-resolution inductively coupled plasma mass spectrometry (HR-ICP-MS) after HNO3 hotplate and microwave digestions. Furthermore, Ag-spiking experiments were conducted with three mushroom species containing 860, 6200, and 21,000 mg Cl kg-1 in dry mass and Ag was determined by HR-ICP-MS after HNO3 hotplate digestion of the samples. Finally, ten replicates of Ag-hyperaccumulating Amanita strobiliformis were analyzed by two variants of INAA utilizing 108Ag in the first step and 110 mAg isotope in the second step. In addition, four additional digestion procedures followed by HR-ICP-MS and inductively coupled plasma optical emission spectroscopy (ICP-OES) measurements of Ag were performed on this A. strobiliformis sample. Analytical quality was controlled by using NIST Standard Reference Materials 1566b (Oyster Tissue) and 2781 (Domestic Sludge). The results of all experiments revealed that correct determination of Ag in mushrooms is not always possible using standard digestion procedures because of precipitation of insoluble AgCl which was documented by scanning electron microscopy and confirmed by the X-ray diffraction analysis.

Czech Academy of Sciences Institute of Geology Rozvojová 269 16500 Prague 6 Czech Republic

Czech Academy of Sciences Nuclear Physics Institute Hlavní 130 25068 Husinec Řež Czech Republic

Institute of Geochemistry Mineralogy and Mineral Resources Faculty of Science Charles University Prague Albertov 6 12843 Prague 2 Czech Republic

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Gadd GM (2013) Geomycology: fungi as agents of biogeochemical change. Biol Environ: Proc R Ir Acad. 10.1353/bae.2013.0006

Stijve T, Cardinale E (1974) Selenium and mercury content of some edible mushrooms. Trav Chim Aliment Hyg. 10.5169/seals-983703

Drbal K, Kalač P, Šeflová A, Šefl J (1975) Content of the trace elements iron and manganese in some edible mushrooms [In Czech]. Česká Mykol 29:110–114 DOI

Drbal K, Kalač P, Šeflová A, Šefl J (1975) Content of copper in some edible mushrooms [In Czech]. Česká Mykol 29:184–186 DOI

Allen RO, Steinnes E (1978) Concentrations of some potentially toxic metals and other trace elements in wild mushrooms from Norway. Chemosphere. 10.1016/0045-6535(78)90138-8

Byrne AR, Dermelj M, Vakselj T (1979) Silver accumulation by fungi. Chemosphere. 10.1016/0045-6535(79)90043-2

Stijve T, Besson R (1976) Mercury, cadmium, lead, and selenium content of mushroom species belonging to the genus

Seeger R, Meyer E, Schönhut S (1976) Lead in mushrooms [In German]. Z Lebensm Unters–Forsch. 10.1007/BF01104354 PubMed

Schmitt JA, Meisch HU, Reinle W (1978) Heavy metals in higher fungi, IV. Silver [In German]. Z Naturforsch C. 10.1515/znc-1978-9-1001

Kuehnelt D, Goessler W, Irgolic KJ (1997) Arsenic compounds in terrestrial organisms I:

Kuehnelt D, Goessler W, Irgolic KJ (1997) Arsenic compounds in terrestrial organisms II: arsenocholine in the mushroom

Michelot D, Siobud E, Doré JC, Viel C, Poirier F (1998) Update on metal content profiles in mushrooms – toxicological implications and tentative approach to the mechanisms of bioaccumulation. Toxicon. 10.1016/s0041-0101(98)00131-7 PubMed

Falandysz J, Kunito T, Kubota R, Brzostowski A, Mazur A, Falandysz JJ, Tanabe S (2007) Selected elements of poison pax PubMed

Falandysz J, Kunito T, Kubota R, Lipka K, Mazur A, Falandysz JJ, Tanabe S (2007) Selected elements in fly agaric PubMed

Meisch HU, Schmitt JA, Reinle W (1977) Heavy metals in higher fungi. Cadmium, zinc and copper [In German]. Z Naturforsch C. 10.1515/znc-1977-3-405

Alonso J, Salgado MJ, García MA, Melgar MJ (2000) Accumulation of mercury in edible macrofungi: influence of some factors. Arch Environ Contam Toxicol. 10.1007/s002449910020 PubMed

Koch E, Kneifel H, Bayer E (1987) Occurrence of amavadin in mushrooms of the genus

Stijve T, Vellinga EC, Herrmann A (1990) Arsenic accumulation in some higher fungi. Persoonia. 14:161–166. https://repository.naturalis.nl/pub/531714/PERS1990014002003.pdf

Borovička J, Řanda Z, Jelínek E (2005) Gold content of ectomycorrhizal and saprobic macrofungi from non–auriferous and unpolluted areas. Mycol Res. 10.1017/s095375620500328x PubMed

Borovička J, Dunn CE, Gryndler M, Mihaljevič M, Jelínek E, Rohovec J, Rohošková M, Řanda Z (2010) Bioaccumulation of gold in macrofungi and ectomycorrhizae from the vicinity of the Mokrsko gold deposit, Czech Republic. Soil Biol Biochem. 10.1016/j.soilbio.2009.10.003

Borovička J, Kotrba P, Gryndler M, Mihaljevič M, Řanda Z, Rohovec J, Cajthaml T, Stijve T, Dunn CE (2010) Bioaccumulation of silver in ectomycorrhizal and saprobic macrofungi from pristine and polluted areas. Sci Total Environ. 10.1016/j.scitotenv.2010.02.031 PubMed

Lepp NW, Harrison SCS, Morrell BG (1987) A role of PubMed

Thomet U, Vogel E, Krähenbühl U (1999) The uptake of cadmium and zinc by mycelia and their accumulation in mycelia and fruiting bodies of edible mushrooms. Eur Food Res Technol. 10.1007/s002170050502

Borovička J, Braeuer S, Walenta M, Hršelová H, Leonhardt T, Sácký J, Kaňa A, Goessler W (2022) A new mushroom hyperaccumulator: cadmium and arsenic in the ectomycorrhizal basidiomycete PubMed

Sácký J, Černý J, Šantrůček J, Borovička J, Leonhardt T, Kotrba P (2021) Cadmium hyperaccumulating mushroom PubMed

Borovička J, Braeuer S, Sácký J, Kameník J, Goessler W, Trubač J, Strnad L, Rohovec J, Leonhardt T, Kotrba P (2019) Speciation analysis of elements accumulated in PubMed

Borovička J, Sácký J, Kaňa A, Walenta M, Ackerman L, Braeuer S, Leonhardt T, Hršelová H, Goessler W, Kotrba P (2023) Cadmium in the hyperaccumulating mushroom PubMed

Braeuer S, Borovička J, Kameník J, Prall E, Stijve T, Goessler W (2020) Is arsenic responsible for the toxicity of the hyperaccumulating mushroom PubMed

Braeuer S, Walenta M, Steiner L, Goessler W (2021) Determination of the naturally occurring vanadium–complex amavadin in

Borovička J, Řanda Z, Jelínek E, Kotrba P, Dunn CE (2007) Hyperaccumulation of silver by PubMed

Borovička J, Konvalinková T, Žigová A, Ďurišová J, Gryndler M, Hršelová H, Kameník J, Leonhardt T, Sácký J (2019) Disentangling the factors of contrasting silver and copper accumulation in sporocarps of the ectomycorrhizal fungus PubMed

Beneš V, Hložková K, Matěnová M, Borovička J, Kotrba P (2016) Accumulation of Ag and Cu in PubMed

Osobová M, Urban V, Jedelský PL, Borovička J, Gryndler M, Ruml T, Kotrba P (2011) Three metallothionein isoforms and sequestration of intracellular silver in the hyperaccumulator PubMed

Hložková K, Matěnová M, Žáčková P, Strnad H, Hršelová H, Hroudová M, Kotrba P (2016) Characterization of three distinct metallothionein genes of the Ag-hyperaccumulating ectomycorrhizal fungus PubMed

Gryndler M, Hršelová H, Soukupová L, Borovička J (2012) Silver release from decomposed hyperaccumulating PubMed

Řanda Z, Soukal L, Mzera J (2005) Possibilities of the short-term thermal and epithermal neutron activation for analysis of macromycetes (mushrooms). J Radioanal Nucl Chem. 10.1007/s10967-005-0676-y

Petrini O, Cocchi L, Vescovi L (2009) Chemical elements in mushrooms: their potential taxonomic significance. Mycol Progress. 10.1007/s11557-009-0589-1

Horák Z, Kučera J, Mizera J, Kameník J, Fikrle M (2024) Modernized control of a pneumatic facility for short-time NAA at LVR-15 reactor in Řež, Czech Republic. J Radioanal Nucl Chem. 10.1007/s10967-023-09146-2

Ferreux L, Lépy MC, Bé MM, Isnard H, Lourenço V (2014) Photon emission intensities in the decay of PubMed

Nakamura S, Wada H, Shcherbakov O, Furutaka K, Harada H, Katoh T (2003) Measurement of the thermal neutron capture cross section and the resonance integral of the

Řanda Z, Kučera J (2004) Trace elements in higher fungi (mushrooms) determined by activation analysis. J Radioanal Nucl Chem. 10.1023/b:jrnc.0000015813.27926.32

Daskalakis KD, O'Connor TP, Crecelius EA (1997) Evaluation of digestion procedures for determining silver in mussels and oysters. Environ Sci Technol. 10.1021/es9608959

Falandysz J, Bona H, Danisiewicz D (1994) Silver uptake by PubMed

Falandysz J, Bona H, Danisiewicz D (1994) Silver content of wild-grown mushrooms from Northern Poland. Z Lebensm Unters Forch. 10.1007/BF01193449 PubMed

Falandysz J & Danisiewicz D (1995) Bioconcentration factors (BCF) of silver in wild PubMed

Joerger R, Klaus T, Pettersson J, Granqvist CG (2000) Digestion method for silver accumulated in micro-organisms. Fresenius J Anal Chem. 10.1007/s002160050060 PubMed

Niazi SB, Littlejohn D, Halls DJ (1993) Rapid partial digestion of biological tissues with nitric acid for the determination of trace elements by atomic spectrometry. Analyst. 10.1039/AN9931800821 PubMed

Sánchez López FJ, Gil Garcia MD, Sánchez Morito NP, Martínez Vidal JL (2003) Determination of heavy metals in crayfish by ICP-MS with a microwave-assisted digestion treatment. Ecotoxicol Environ Safety. 10.1016/S0147-6513(02)00050-7 PubMed

Huang L, Bell RW, Dell B, Woodward J (2004) Rapid nitric acid digestion of plant material with an open-vessel microwave system. Commun Soil Sci Plant Anal. 10.1081/CSS-120029723

Tarantino TB, Barbosa IS, de Lima C, Pereira MG, Teixeira LSG, Korn MGA (2017) Microwave-assisted digestion using diluted nitric acid for multi-element determination in rice by ICP-OES and ICP-MS. Food Anal Methods. 10.1007/s12161-016-0658-4

Greene CH, Frizzell LD (1936) Studies of the precipitation of silver chloride. II. From silver nitrate and hydrochloric acid. J Am Chem Soc. 10.1021/ja01294a036

D’Elia CF, Sanders JG, Capone DG (1989) Analytical chemistry for environmental sciences. A question of confidence. Environ Sci Technol. 10.1021/es00065a005

Crecelius EA, Daskalakis K (1994) Analysis of silver in mussels and oysters by inductively couple plasma mass spectrometry (ICPMS). In proceedings: Transport, fate and effects of silver in the environment. pp. 157–160.

Mizera J, Řanda Z, Kučera J (2008) Determination of silver in biological reference materials by neutron activation analysis. J Radioanal Nucl Chem. 10.1007/s10967-008-1101-0

Poitras EP, Levine MA, Harrington JM, Amal SE, Fennell TR, Snyder RW, Black SL, Summer SS, Levine KE (2015) Development of an analytical method for assessment of silver nanoparticle content in biological matrices by inductively coupled plasma mass spectrometry. Biol Trace Elem Res. 10.1007/s12011-014-0141-2 PubMed PMC

Yang XJ, Foley R, Low GKC (2002) A modified digestion procedure for analysing silver in environmental water samples. Analyst. 10.1039/b109959k

Rahfeld A, Wiehl N, Dressler S, Möckel R, Gutzmer J (2018) Major and trace element geochemistry of the European Kupferschiefer – an evaluation of analytical techniques

Kimbrough DE, Wakakuwa JR (1989) Acid digestion for sediments, sludges, soils, and solid wastes. A proposed alternative to EPA SW 846 Method 3050. Environ Sci Technol. 10.1021/es00065a021

Chen Y, Mao Y, Song M, Yin Y, Liu G, Cai Y (2020) Occurrence and leaching of silver in municipal sewage sludge in China. Ecotoxicol Environ Saf. 10.1016/j.ecoenv.2019.109929 PubMed

Coutris C, Joner EJ, Oughton DH (2012) Aging and soil organic matter content affect the fate of silver nanoparticles in soil. Sci Total Environ. 10.1016/j.scitotenv.2012.01.027 PubMed

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. 10.1016/j.envpol.2016.08.009 PubMed

Wang P, Menzies NW, Chen H, Yang X, McGrath SP, Zhao FJ, Kopittke PM (2018) Risk of silver transfer from soil to the food chain is low after long-term (20 years) field applications of sewage sludge. Environ Sci Technol. 10.1021/acs.est.8b00204 PubMed

Fernández-Caliani JC, Giráldez MI, Rivera MB (2019) Source and geochemical partitioning of silver in a naturally-enriched soil. Appl Geochem. 10.1016/j.apgeochem.2019.02.010

Byrne AR, Kučera J (1997) Role of the self-validation principle of NAA in the quality assurance of bioenvironmental studies and in the certification of reference materials. In proceedings: International Atomic Energy Agency. pp. 223–238. https://inis.iaea.org/search/29019696

Stijve T, Andrey D, Lucchini G, Goessler W (2002) Lanthanides and other less common metals in mushrooms. Deut Lebensm-Rundsch 98(3):82–87

Komárek M, Chrastný V, Štíchová J (2007) Metal/metalloid contamination and isotopic composition of lead in edible mushrooms and forest soils originating from a smelting area. Environ Int. 10.1016/j.envint.2007.02.001 PubMed

Drewnowska M, Falandysz J, Chudzińska M, Hanć A, Saba M, Barałkiewicz D (2017) Leaching of arsenic and sixteen metallic elements from

Falandysz J, Drewnowska M, Chudzińska M, Barałkiewicz D (2017) Accumulation and distribution of metallic elements and metalloids in edible PubMed

Falandysz J, Hanć A, Barałkiewicz D, Zhang J, Treu R (2020) Metallic and metalloid elements in various developmental stages of PubMed

Zhang J, Barałkiewicz D, Hanć A, Falandysz J, Yuanzhong W (2020) Contents and health risk assessment of elements in three edible ectomycorrhizal fungi ( PubMed

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. 10.1080/02652030119625 PubMed

Kubrová J, Žigová A, Řanda Z, Rohovec J, Gryndler M, Krausová I, Dunn CE, Kotrba P, Borovička J (2014) On the possible role of macrofungi in the biogeochemical fate of uranium in polluted forest soils. J Hazard Mater. 10.1016/j.jhazmat.2014.07.050 PubMed

Sácký J, Liščáková V, Šnábl J, Zelenka J, Borovička J, Leonhardt T, Kotrba P (2025) Functional analysis of two genes coding for distinct cation diffusion facilitators of the cadmium-accumulating fungus PubMed

Jones KC, Peterson PJ, Davies BE, Minski MJ (1985) Determination of silver in plants by flameless atomic absorption spectrometry and neutron activation analysis. Int J Environ Anal Chem. 10.1080/03067318508078368

Krejsa J, Šíma J, Kobera M, Šeda M, Svoboda L (2021) Detrimental and essential elements in fruiting bodies of mushrooms with ecological relationship to birch ( PubMed

Siobud-dorocant E, Doré JC, Michelot D, Poirier F, Viela C (1999) Multivariate analysis of metal concentration profiles in mushrooms. SAR and QSAR in Environ Res. 10.1080/10629369908039104 PubMed

Brzostowski Y, Falandysz J, Jarzyńska G, Zhang D (2011) Bioconcentration potential of metallic elements by poison pax ( PubMed

Kułdo E, Jarzyńska G, Gucia M, Falandysz J (2014) Mineral constituents of edible parasol mushroom

Kojta AK, Gucia M, Krasińska G, Saba M, Nnorom IC, Falandysz J (2016) Mineral constituents of edible field parasol (

Lipka K, Falandysz J (2017) Accumulation of metallic elements by PubMed

Falandysz J, Treu R (2019)

Falandysz J, Treu R, Meloni D (2021) Distribution and bioconcentration of some elements in the edible mushroom PubMed

Mleczek M, Budka A, Kalač P, Siwulski M, Niedzielski P (2021) Family and species as determinants modulating mineral composition of selected wild-growing mushroom species. Environ Sci Pollut Res. 10.1007/s11356-020-10508-6 PubMed PMC

Borovička J, Braeuer S, Žigová A, Gryndler M, Dima B, Goessler W, Frøslev TG, Kameník J, Kärcher R (2017) Resurrection of PubMed PMC

Alaimo MG, Dongarrà G, La Rosa A, Tamburo E, Vasquez G, Varrica D (2018) Major and trace elements in PubMed

Mleczek M, Siwulski M, Mikołajczak P, Goliński P, Gąsecka M, Sobieralski K, Dawidowicz L, Szymańczyk M (2015) Bioaccumulation of elements in three selected mushroom species from southwest Poland. J Environ Sci Health Pestic Food Contam Agri. 10.1080/03601234.2015.982427 PubMed

Anderson P, Davidson CM, Littlejohn D, Ure AM, Shand CA, Cheshire MV (1996) The determination of caesium and silver in soil and fungal fruiting bodies by electrothermal atomic absorption spectrometry. Anal Chim Acta. 10.1016/0003-2670(96)00069-4

Anderson P, Davidson CM, Littlejohn D, Ure AM, Shand CA, Cheshire MV (1997) The translocation of caesium and silver by fungi in some Scottish soils. Commun Soil Sci Plan. 10.1080/00103629709369816

Stefanović V, Trifković J, Djurdjić S, Tešić Ž, Mutić J (2016) Study of silver, selenium and arsenic concentration in wild edible mushroom PubMed

Vukojević V, Đurđić S, Mutić J (2019) Accumulation of U, Th, Pb, V, Rb, and Ag in wild mushrooms PubMed DOI

Krejsa J, Šíma J, Křížek M, Šeda M, Svoboda L (2024) Selected detrimental and essential elements in fruiting bodies of culinary and toxic medicinal macroscopic fungi growing in the bohemian forest, the Czech republic. J Environ Sci Health B. 10.1080/03601234.2024.2362548 PubMed

Parisis NE, Van Den Heede MA (1992) Antimony uptake and correlation with other metals in mushroom species. Toxicol Environ Chem. 10.1080/02772249209357843

Demirbaş A (2001) Concentrations of 21 metals in 18 species of mushrooms growing in the east black sea region. Food Chem. 10.1016/S0308-8146(01)00236-9

Aruguete DM, Aldstadt JH, Mueller GM (1998) Accumulation of several heavy metals and lanthanides in mushrooms (

Horovitz CT, Schock HH, Horovitz-Kisimova LA (1974) The content of scandium, thorium, silver, and other trace elements in different plant species. Plant Soil. 10.1007/BF00011522

Hedrich E (1988) Short-time activation analysis of some Austrian mushrooms. J Trace Microprobe Tech 6(4):583–602

Sácký J, Leonhardt T, Borovička J, Gryndler M, Briksí A, Kotrba P (2014) Intracellular sequestration of zinc, cadmium and silver in PubMed

Borovička J, Bušek B, Mikšík M, Dvořák D, Jeppesen TS, Dima B, Albert L, Frøslev TG (2015)

Wolfe BE, Tulloss RE, Pringle A (2012) The irreversible loss of a decomposition pathway marks the single origin of an ectomycorrhizal symbiosis. PLoS One. 10.1371/journal.pone.0039597 PubMed PMC

Varga D, Hanss JM, Moreau PA, Kovács GM, Dima B (2024) Phylogenetic and morphological studies reveal large diversity and three new species in

Zelyanskii AV, Zhukova LV, Kitaev GA (2001) Solubility of AgCl and AgBr in HCl and HBr. Inorg Mater. 10.1023/A:1017597321655

Luo Y, Celo V, Dabek-Zlotorzynska E, Yang L (2012) Effects of precipitation and UV photolysis on Ag isotope ratio: experimental studies. J Anal At Spectrom. 10.1039/C1JA10291E