Boletus edulis mushroom behaved as an accumulating biosystem with respect to Ag, Rb, Zn, and K. The mushroom was not an efficient accumulator of toxic As, Pb, and Cr, but Se and Cd displayed much higher concentrations in the mushroom than in the substrate samples. Other elements were bioexclusive. Different elements had different within-mushroom mobilities. The highest mobilities were displayed by Zn and Ag, and the lowest by Ti. The mushroom's fruiting body preferentially took up lighter Mg, Cu, and Cd isotopes (Δ26MgFB-soil = -0.75‰; Δ65CuFB-soil = -0.96‰; Δ114CdFB-soil = -0.63‰), and the heavier 66Zn isotope (Δ66ZnFB-soil = 0.92‰). Positive within-mushroom Zn isotope fractionation resulted in accumulation of the heavier 66Zn (Δ66Zncap-stipe = 0.12‰) in the mushroom's upper parts. Cadmium displayed virtually no within-mushroom isotope fractionation. Different parts of the fruiting body fractionated Mg and Cu isotopes differently. The middle part of the stipe (3-6 cm) was strongly depleted in the heavier 26 Mg with respect to the 0-3 cm (Δ26Mgstipe(3-6)-stipe(0-3) = -0.73‰) and 6-9 cm (Δ26Mgstipe(6-9)-stipe(3-6) = 0.28‰) sections. The same stipe part was strongly enriched in the heavier 65Cu with respect to the 0-3 cm (Δ65Custipe(3-6)-stipe(0-3) = 0.63‰) and 6-9 cm (Δ65Custipe(6-9)-stipe(3-6) = -0.42‰) sections. An overall tendency for the upper mushroom's parts to accumulate heavier isotopes was noted for Mg (Δ26Mgcap-stipe = 0.20‰), Zn (Δ66Zncap-stipe = 0.12‰), and Cd (Δ114Cdcap-stipe = 0.04‰), whereas Cu showed the opposite trend (Δ65Cucap-stipe = -0.08‰).

Division of Geochemistry and Laboratories Czech Geological Survey Geologicka 6 15200 Prague Czech Republic

Zobrazit více v PubMed

Andronikov AV, Andronikova IE, Sebek O. First data on trace element and isotope compositions of a Xerocomus subtomentosus mushroom from western Czech Republic. Environ Sci Pollut Res. 2022;29:9369–9374. PubMed

Antonin V, Hagara L, Baier J (2019) Otto’s great atlas of the mushrooms. Otto Publishing House, Prague, Czech Republic, 432 pp. (in Czech)

Arnold T, Markovic T, Kirk GJD, Schönbächler M, Rechkämper M, Zhao FJ, Weiss DJ. Iron and zinc isotope fractionation during uptake and translocation in rice (Oryza sativa) grown in oxic and unoxic soils. Comptes Rendus Geosci. 2015;347:397–404.

Arnott HJ. Calcium oxalate in fungi. In: Khan SR, editor. Calcium oxalate in biological systems. Boca Raton: CRC Press; 1995. pp. 73–111.

Benes V, Leonhardt T, Kana A, Sacky J, Kotrba P. Heterologus expression of Zn-binding peptide RaZBP1 from Russula bresadolae does not overcome Zn and Cd detoxification mechanisms in Hebeloma mesophaeum. Folia Microbiol. 2019;64:835–844. PubMed

Black JR, Epstein E, Rains WD, Yin QZ, Casey WH. Magnesium-isotope fractionation during plant growth. Environ Sci Technol. 2008;42:7831–7836. PubMed

Blotevogel S, Schreck E, Audry S, Saldi GD, Viers J, Courjault-Rade P, Darrozes J, Orgogozo L, Olivia P. Contribution of soil elemental contents and Cu and Sr isotope ratios to the understanding of pedogenic processes and mechanisms involved in the soil-to-grape transfer (Soave vineyard, Italy) Geoderma. 2019;343:72–85.

Blotevogel S, Olivia P, Denaix L, Audry S, Viers J, Schreck E (2022) Stable Cu Isotope Ratios Show Changes in Cu Uptake and Transport Mechanisms in Vitis vinifera Due to High Cu Exposure. Frontiers Plant Sci 12, Sec Plant Nutrition:755944, 10.3389/fpls.2021.755944 PubMed PMC

Bolou-Bi EB, Pozswa A, Leyval C, Vigier N. Experimental determination of magnesium isotope fractionation during higher plant growth. Geochim Cosmochim Acta. 2010;74:2523–2537.

Bolou-Bi EB, Vigier N, Pozswa A, Boudot J-P, Dambrine E. Effects of biochemical processes on magnesium isotope variations in a forested catchment in the Vosges Mountains (France) Geochim Cosmochim Acta. 2012;87:341–355.

Borovicka J, Sacky J, Kana A, Walenta M, Ackerman L, Braeuer S, Leonhardt T, Hrselova H, Goessler W, Kotrba P. Cadmium in the hyperaccumulating mushroom Thelephora pinicillata: intracellular speciation and isotopic composition. Sci Total Environ. 2022;855:159002. PubMed

Brenot A, Cloquet C, Vigier N, Carignan J, France-Lanord C. Magnesium isotope systematics of the lithologically varied Moselle river basin, France. Geochim Cosmochim Acta. 2008;72:5070–5082.

Burford EP, Fomina M, Gadd GM. Fungal involvement in bioweathering and biotransformation of rocks and minerals. Mineral Mag. 2003;67:1127–1155.

Busuioc G, Elekes CC, Stihi C, Iordache S, Ciulei SC. The bioaccumulation and translocation of Fe, Zn, and Cu in species of mushrooms from Russula genus. Environ Sci Pollut Res. 2011;18:890–896. PubMed

Cadiou JL, Pichat S, Bondanese VP, Soulard A, Fujii T, Albarede E, Oger P. Copper transporters are responsible for copper isotopic fractionation in eukaryotic cells. Sci Reps. 2017;7:44533. PubMed PMC

Chen S, Liu Y, Hu J, Zhang Z, Hou Z, Huang F, Yu H. Zinc isotopic composition of NIST SRM 683 and whole-rock reference materials. Geostand Geoanal Res. 2016;40:417–432.

Chrastny V, Cadkova E, Vanek A, Teper L, Cabala J, Komarek M. Cadmium isotope fractionation within the soil profile complicates source identification in relation to Pb-Zn mining and smelting processes. Chem Geol. 2015;405:1–9.

Criss RE. Principles of stable isotope distributions. New York: Oxford University Press; 1999. p. 254.

Dumay QC, Debut AJ, Mansour NM, Saier MH Jr (2006) The copper transporter (Ctr) family of Cu+ uptake systems. J Molec Microbiol Biotechnol 11:10–19 PubMed

Durdic S, Stankovic V, Razic S, Mutic J. Lead isotope ratios as tool for elicidation of chemical environment in a system of Macrolepiota procera (Scop.) Singer – soil. Environ Sci Pollut Res. 2021;28:59003–59014. PubMed

Dusemgemungu L, Kasali G, Gwanama C, Mubemba B. Overview of fungal bioleaching of metals. Environ Advances. 2021;5:100083.

Fahad ZA, Bolou-Bi EB, Köhler SJ, Finlay RD, Mahmood S. Fractionation and assimilation of Mg isotopes by fungi is species dependant. Environ Microbiol Reps. 2016;8:956–965. PubMed

Falandysz J, Drevnovska M, Chudzinska M, Baralkiewicz D. Accumulation and distribution of metallic elements and metalloids in edible Amanita fulva mushrooms. Ecotoxicology Environ Safety. 2017;137:265–271. PubMed

Filipiak M, Filipiak ZM. Application of ionomics and ecological stoichiomentry in conservation biology: nutrient demand and supply in a changing environment. Biol Conserv. 2022;272:109622.

Fomina MA, Alexander IJ, Hillier S, Gadd GM. Zinc phosphate and pyromorphite solubilization by soil plant-symbiotic fungi. Geomicrobiol J. 2004;21:351–366.

Gadd GM. Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol Res. 2007;111:3–49. PubMed

Gadd GM (2017) The geomycology of elemental cycling and transformations in the environment. Microbiol Spectrum 5:FUNK-0010–2016 PubMed PMC

Gadd GM, Bahri-Esfahani J, Li Q, Rhee YJ, Wei Z, Fomina M, Liang X. Oxalate production by fungi: significance in geomycology, biodeterioration and bioremediation. Fungal Biol Rev. 2014;28:36–55.

Galy A, Yoffe O, Janney PE, Williams RW, Cloquet C, Alard O, Halicz L, Wadhwa M, Hutcheon ID, Ramon E, Carihnan J. Magnesium isotope heterogeneity of the isotopic standard SRM 980 and new reference materials for magnesium isotope ratio measurements. J Anal Atom Spectrom. 2003;18:1352–1356.

Hindshaw RS, Reynolds BC, Wiederhold JG, Kiczka M, Kretzschmar R, Bourdon B. Calcium isotope fractionation in alpine plants. Biogeochem. 2013;112:373–388.

Hobbie EA, Högberg P. Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics. New Phytol. 2012;196:367–382. PubMed

Imseng M, Wiggenhauser M, Keller A, Muller M, Rehkamper M, Murphy K, Kreissig K, Frossard E, Wilcke W, Bigalke M. Towards the understanding of the Cd isotope fractionation during transfer from the soil to the cereal grain. Environ Pollut. 2019;244:834–844. PubMed

Jouvin D, Weis DJ, Mason TFM, Bravin BM, Louvat P, Zhao F, Ferec F, Hinsinger P, Benedeti MF. Stable isotopes of Cu and Zn in higher pants: evidence for Cu reduction at the root surface and two conceptual models for isotopic fractionation processes. Environ Sci Technol. 2012;46:2652–2660. PubMed

Kalac P. Chemical composition and nutritional value of European species of wild growing mushrooms: a review. Food Chem. 2009;113:9–16.

Kalac P, Svoboda L. A review of trace element concentrations in edible mushrooms. Food Chem. 2000;69:273–281.

Kaspari M. The invisible hand of the periodic table: how micronutrients shape ecology. Ann Rev Ecol Evol System. 2021;52:199–219.

Kaspari M, Powers JS. Biogeochemistry and geographic ecology: embracing all twenty five elements required to build organisms. Am Nat. 2016;188:S62–73. PubMed

Kavner A, John SG, Sass S, Boyle EA. Redox-driven stable isotope fractionation in transition metals: application to Zn electroplating. Geochim Cosmochim Acta. 2008;72:1731–1741.

Kendall C, Doctor DH (2003) Stable isotope applications in hydrologic studies. In: Holland HD and Turekian KK (eds) Treatise on Geochemistry 5, Elsevier, pp 319–364. 10.1016/B0-08-043751-6/05081-7

Knauerova M, Slavicik J, Urubova L (2020) Atlas of the mushrooms (a guide to the Czech nature). Edika Publishing House, Prague, Czech Republic, 152 pp. (in Czech)

Kojta AK, Gucia M, Krasinska G, Saba M, Norom IC, Falandyzs J. Mineral constituents of edible parasol (Macrolepiota procera) mushrooms and the underlying substrate from upland regions of Poland: bioconcentration potential, intake benefits, and toxicological risk. Polish J Environ Stud. 2016;25:1–16.

Kříbek B, Míková J, Knésl I, Mihaljevič M, Sýkorová I. Uptake of trace elements and isotope fractionation of Cu and Zn by birch (Betula pendula) growing on mineralized coal waste pile. App Geochem. 2020;122:104741.

Landweert R, Hoffland E, Finlay RD, Kuyper TW, van Breemen N. Linking plants to rocks: ectomycorrhizal fungi mobilized nutrients from minerals. TRENDS Ecol Evol. 2001;16:248–254. PubMed

Li S-Z, Zhu X-K, Wu L-H, Luo Y-M. Cu isotopic compositions in Elsholtzia splendens: Influence of soil condition and growth period on Cu isotopic fractionation in plant tissue. Chem Geol. 2016;444:49–58.

Liu M-S, Zhang Q, Zhang Y, Zhang Z, Huang F, Yu H-M. High-precision Cd isotope measurements of soil and rock reference materials by MC-ICP-MS with double-spike correction. Geostand Geoanal Res. 2020;44:169–182.

Makishima A, Nakamura E. Low-blank chemistry for Zn stable isotope ratio determination using extraction chromatographic resin and double spike-multiple collector-ICP-MS. J Anal Atom Spectrom. 2013;28:127–133.

Mallikarjuna SE, Ranjini A, Haware DJ, Viyaialaksmi MR, Shashirekha MN, Rajarathnam S. Mineral composition of four edible mushrooms. J Chem. 2013;2013:1–5.

Martinkova E, Chrastny V, Francova M, Sipkova A, Curik J, Myska O, Mizic L. Cadmium isotope fractionation of materials derived from various industrial processes. J Hazard Mater. 2016;302:114–119. PubMed

Martino E, Perotto S, Parsons R, Gadd GM. Solubilization of insoluble inorganic zinc compounds by ericoid mycorrhizal fungi derived from heavy metal polluted sites. Soil Biol Biochem. 2003;8:409–413.

Moeller K, Schoenberg R, Pedersen R-B, Weiss D, Dong S. Calibration of new certified reference materials ERM-AE633 and ERM-AE647 for copper and IRMM-3702 for zinc isotope amount ratio determination. Geostand Geoanal Res. 2012;36:177–199.

Moynier F, Pichat S, Pons M-L, Fike D, Balter V, Albaréde F. Isotopic fractionation and transport mechanisms of Zn in plants. Chem Geol. 2009;267:125–130.

Navarette JU, Borrok DM, Viveros M, Ellzey JT. Copper isotope fractionation during surface adsorption and intracellular incorporation by bacteria. Geochim Cosmochim Acta. 2011;75:784–799. PubMed PMC

Nordberg GF, Bernard A, Diamond GL, Duffus JH, Illing P, Nordberg M, Bergdahl IA, Jin T, Skerfving S. Risk assessment of effects of cadmium on human health (IUPAC technical report) Pure App Chem. 2018;90:755–808.

Novak M, Sipkova A, Chrastny V, Stepanova M, Voldrichova P, Veselovsky F, Prechova E, Blaha V, Curik J, Farkas J, Erbanova L, Bohdalkova L, Pasava J, Mikova J, Komarek A, Krachler M. Cu-Zn isotope constraints on the provenance of air pollution in Central Europe: Using soluble and insoluble particles in snow and rime. Environ Pollut. 2016;218:1135–1146. PubMed

Novak M, Kram P, Sebek O, Andronikov AV, Chrastny V, Martinkova E, Stepanova M, Prechova E, Curik J, Veselovsky F, Myska O, Stedra V, Farkas J. Temporal changes in Cr fluxes and δ53Cr values in runoff from a small serpentinite catchment (Slavkov Forest, Czech Republic) Chem Geol. 2017;472:22–30.

Novak M, Farkas J, Kram P, Hruska J, Stepanova M, Veselovsky F, Curik J, Andronikov AV, Sebek O, Simecek M, Fottova D, Bohdalkova L, Prechova E, Koubova M, Vitkova H. Controls on δ26Mg variability in three Central European headwater catchments characterized by contrasting bedrock chemistry and contrasting inputs of atmospheric pollutants. PLOS One. 2020;15:e0242915. doi: 10.1371/journal.pone.0242915. PubMed DOI PMC

Pokharel R, Gerrits R, Schuessler JA, Floor GH, Gorbushina AA, von Blankenburg F (2017) Mg isotope fractionation during uptake by a rock-inhabiting, model microcolonial fungus Knufia petricola at acidic and neutral pH. Environ Sci Technol 51:9691–9699 PubMed

Pokharel R, Gerrits R, Schuessler JA, Frings PJ, Sobotka R, Gorbushina AA, von Blankenburg F. Magnesium stable isotope fractionation on a cellular level explored by cyanobacteria and black fungi with implications for higher plants. Environ Sci Technol. 2018;52:12216–12224. PubMed

Ryan BM, Kirby JK, Degryse F, Harris H, McLaughlin MJ, Scheiderich K. Copper speciation and isotopic fractionation in plants: uptake and translocation mechanisms. New Phytol. 2013;199:367–378. PubMed

Sacky J, Chaloupecka A, Kana A, Santrucek J, Borovicka J, Leonhardt T, Kotrba P. Intracellular sequestration of cadmium and zinc in ectomycorrhizal fungus Amanita muscaria (Agaricales, Amanitaceae) and characterization of its metallothionine gene. Fungal Genetics Biol. 2022;162:103717. PubMed

Shalev N, Farkas J, Fietzke J, Novak M, Schuessler JA, Pogge von Strandmann PAE, Torber PB. Mg isotope interlaboratory comparison of reference materials from earth-surface low-temperature environments. Geostand Geoanal Res. 2018;42:205–221.

Shearer G, Kohl DH. N2-fixation in field settings: estimations based on natural 15N abundance. Austral J Plant Physiol. 1986;13:699–756.

Sossi PA, Halverson GP, Nebel O, Eggins SM. Combined separation of Cu, Fe and Zn from rock matrices and improved analytical protocols for stable isotope determination. Geostand Geoanal Res. 2015;39:129–149.

Strnad L, Mihaljevič M, Šebek O. Laser ablation and solution ICP-MS determinations of REE in USGS BIR-1G, BHVO-2G and BCR-2G glass reference materials. Geostand Geoanal Res. 2005;29:303–314.

Svoboda L, Chrastny V. Levels of eight trace elements in edible mushrooms from a rural area. Food Addit Contam: Part A. 2008;25:51–58. PubMed

Teng F-Z, Dauphas N, Watkins JM. Non-traditional stable isotopes: retrospective and prospective. Rev Mineral Geochem. 2017;82:1–26.

Thornton I (1986) Geochemistry of cadmium. In: Mislin H, Ravera O (eds.), Cadmium in the Environment. Experientia Supplementum 50, Birkhauser Basel, pp 7–12

Uhlig D, Schuessler JA, Bouchez J, Dixon JL, von Blankenburg F. Quantifying nutrient uptake as driver of rock weathering in forest ecosystems by magnesium stable isotopes. Biogeosci. 2017;14:3111–3128.

Viers J, Oliva P, Nonell A, Gelabert A, Sonke JE, Freydier R, Gainville R, Dupre B. Evidence of Zn isotopic fractionation in a soil-plant system of a pristine tropical watershed (Nsimi, Cameroon) Chem Geol. 2007;239(124):137.

Voldrichova P, Chrastny V, Sipkova A, Farkas J, Novak M, Stepanova M, Krachler M, Veselovsky F, Blaha V, Prechova E, Komarek A, Bohdalkova L, Curik J, Mikova J, Erbanova L, Pacherova P. Zinc isotope systematics in snow and ice accretions in Central European mountains. Chem Geol. 2014;388:130–141.

Walker GM, White NA (2018) Introduction to Fungal Physiology. In: Kavangh K (ed) Fungi: Biology and Applications, 3rd edn. John Wiley & Sons, Inc., pp 1–35. 10.1002/9781119374312.ch1

Wei R, Guo Q, Wen H, Liu C, Yang J, Peters M, Hu J, Zhu G, Zhang H, Tian L, Han X, Ma J, Zhu C, Wan Y. Fractionation of stable cadmium isotopes in the cadmium tolerant Ricinus communis and hyperaccumulator Solanum nigrum. Sci Reps. 2016;6:24309. PubMed PMC

Weinstein C, Moynier F, Wang K, Paniello R, Foriel J, Catalano J. Cu isotopic fractionation in plants. Chem Geol. 2011;286:266–271.

Weiss DJ, Mason TFD, Zhao FJ, Kirk GJD, Coles BJ, Horstwood MSA. Isotopic discrimination of zinc in higher plants. New Phytol. 2005;165:703–710. PubMed

Wiggenhauser M, Aucour A-M, Telouk P, Blommaert H, Sarret G. Changes in cadmium storage forms and isotope ratios in rice during grain filling. Front Plant Sci. 2021;12:645150. PubMed PMC

Wiggenhauser M, Moore RET, Wang P, Bienert GP, Laursen KH, Blotevogel S. Stable isotope fractionation of metals and metalloids in plants: a review. Front Plant Sci. 2022;13:840941. PubMed PMC

Zhao Y, Li Y, Wiggenhauser M, Yang J, Sarret G, Cheng Q, Liu J, Shi Y. Theoretical isotope fractionation of cadmium in the soil-rice-human continuum. Chem Geol. 2021;571:120178.

Zhou J-W, Li Z, Liu M-S, Wu L-H, Huang F, Luo Y-M, Christie P. Cadmium isotopic fractionation in the soil-plant system during repeated phytoextraction with a cadmium hyperaccumulating plant species. Environ Sci Technol. 2020;54:13598–13609. PubMed

Zhu XK, Guo Y, Williams RJ, O’Nions RK, Matthews A, Belshaw NS, Canters GW, de Waal EC, Weser U, Burgess BK, Salvato B. Mass fractionation processes of transition metal isotopes. Earth Planet Sci Lett. 2002;200:47–62.