Introduction

Fungi are an important component of the biosphere, and their production (micro- and macrofungi) is a rapidly growing sector of the food economy worldwide (Royse et al. 2017). This includes developing countries in Africa, Asia, and Central America where locals, indigenous people, or members of the general public forage for both, fruiting bodies and sclerotia (a dense conglomerate of mycelium produced by some species that serves as a food reserve for the fungus) as a food and also as a therapeutic resource. Dozens of species have been successfully farmed, and there are continuous attempts to domesticate new ones (Wasser 2010; Nnorom et al. 2013; Wang et al. 2013; Thawthong et al. 2014; Santiago et al. 2016; Yongabi 2019). Foraging for wild mushrooms is still popular in Europe, e.g., in Italy, Spain, Czechia, Slovakia, Poland, Turkey, Finland, Lithuania, Switzerland, and France, either as a traditional pastime, a seasonal recreation, or for commercial reasons (Læssoe et al. 1996; Isiloglu et al. 2001; Pelkonen et al. 2006; Stijve 2007; Falandysz and Borovička 2013; Kalać, 2016). Globally, 44.2 million tons of mushrooms were produced in 2021 (FAO 2022), but this does not include the quantities of wild mushrooms that are foraged by individuals for personal consumption or for sale, locally. Button mushrooms (champignon), oyster mushrooms, and shitake are still the most popular commercial varieties and dominate the global consumer market for these foods (FAO 2022).

Mushrooms with edible or medicinal value are highly biodiverse, numerous, and have evolved to colonize a variety of soil and plant substrates. Their position, between the plant and animal kingdoms, bestows a meaty texture and taste to the flesh of many edible species, largely resulting from the occurrence and composition of amino acids (Miller et al. 2014; Jaworska et al. 2015; Kalać, 2016). The possibility of combining traditional knowledge of mushrooms in folk medicine (Grzywnowicz 2007; Wasser 2010; Bhatt et al. 2018), with the requirements of modern pharmacy and the search for new bioactive compounds as possible medicines, is currently a challenging field of research (Money 2016; Gründemann et al. 2020). The successful attempts to domesticate some of these have resulted in a diverse range of farmed species—mainly saprotrophs, which can be raised using a wide variety and composition of substrates (often waste agricultural/plant material) (Koutrotsios et al. 2018; Rizzo et al. 2021; Berger et al. 2022). Complementing this use and biodiversity, fungi are now increasingly explored for bioactive organic and inorganic components and as possible agents for the remediation of contaminated land (Sanchez and Demain 2017; Treu and Falandysz 2017).

This work concisely documents and critically overviews literature data on the occurrence of La and Ce in the fruiting bodies of wild and farmed species of edible and medicinal mushrooms. In particular, the evaluation was based on parameters such as environmental geochemistry, cultivation practice, analytical chemistry, food toxicology, mushroom systematics, and ecology. An initial assessment of any potential health risk from REE intake through mushroom consumption was also made.

Rare-earth elements

Lanthanides, referred to as the rare earth elements (REE; La, Ce, Pr, Nd, Sm, Eu, Gd, Tb, Dy, Ho, Er, Tm, Yb, and Lu), are often reported as light-, medium-, and heavy atomic weight REE. The IUPAC definition also includes Sc and Y, but this inclusion is currently the subject of debate between different scientific disciplines. They are dispersed in soil bedrock, clays, and topsoils and are similarly absorbed from the soil solution by mushrooms and plants, making them amenable to further migration up food webs (Brioschi et al. 2013; Khan et al. 2017; Squadrone et al. 2019; Patel et al. 2023). Within the last few decades, applications of REE in alloys, high-tech materials, and commodities have seen a rapid increase as have the related activities of geological extraction and processing of ores for these metals. REE are increasingly used in modern technologies including magnets in electric motors, metallurgy, the electronics sector, wind turbines, crude oil refining, catalytic converters in the automotive industry, and others (Voncken 2016; Mordor Intelligence 2022). So, in addition to research and investigations into geological resources, production, new applications, inventions, and analytical chemistry, REE also attract growing attention within the environmental, food, and toxicological sciences (Li et al. 2013; Migaszewski and Gałuszka 2016; Doulgeridou et al. 2020; Piarulli et al. 2021; Brouziotis et al. 2022; Falandysz and Fernandes 2023). Typically, REE are present in terrestrial feeds and drinking water at low levels, but the current state of knowledge suggests that they are neither essential nor toxic at current occurrence levels in foods, feeds, and environmental media (Squadrone et al. 2018; Wysocka et al. 2018). From the food toxicology point of view, data on the toxicity of the full range of REE to humans are incomplete, while their occurrence and typical concentrations in plant-based foodstuff are reported as “natural” and without advisories or precautions (Squadrone et al. 2018; Doulgeridou et al. 2020). Recent experiments on toxicity using omics-based approaches (with micro-fungus Saccharomyces cerevisiae) have identified some biological functions and pathways that may be disrupted by some medium and heavy atomic weight REE and also the key genes and proteins that are associated with this mode of toxicity (Pallares et al. 2023). These effects were not identified for the light atomic weight members (Ce, La, and Nd), which have analogous features and can be a substitute for calcium (Ca) in some bacteria. REE data reported so far on matrices from marine environments (macro algae—seaweeds, fish seem to show higher concentrations in marine than terrestrial species, on a dry weight basis) (Squadrone et al. 2017, 2019).

Among the REE, La, Ce, and Nd have seen the most applications. Cerium is largely used to manufacture aluminim alloys and also as a fluid cracking catalyst for oil refineries, a catalyst for self-cleaning ovens, in engineered nanomaterials, a polishing powder for liquid crystal and glass display panel surfaces, magnetic memory discs, a chemical oxidizing agent, as a yellow colorant in glass and ceramics, as ferrocerium flints for lighters, and as robust intrinsically hydrophobic coatings for turbine blades. Lanthanum is used in high refractive index and alkali-resistant glass, flint, hydrogen storage, battery-electrodes, camera, and refractive telescope lenses, and as a fluid catalytic cracking catalyst in oil refineries (Voncken 2016).

CeO2NP and CeO2 are engineered Ce-nanoparticles that are used as model compounds in toxicological studies but have also found agricultural and commercial application, with the potential for nanomedicine (Ma et al. 2023). The pressures of promoting innovation and economy, accompanied by the lack of comprehensive toxicological research on new food additives, raise questions on the risk such as the safety of metal nanoparticles that are used directly in food and taken up orally by humans. Even those that have been used for some time, e.g., TiO2, SiO2, ZnO, Fe2O3, turn out to be problematic and even risky (Cheng et al. 2023).

This increasing and diverse use of REE is considered a potential source of pollution of environmental media including soils (Qvarforth et al. 2022). Airborne REE, (e.g., La, which is one of the most used REE in fluid catalytic cracking catalysts and is released from local sources of emission such as production sites or oil refineries), behave like classical heavy metals, undergoing atmospheric and also wastewater diffusion, and finally fallout or sedimentation on surfaces (Kulkarni et al. 2007; Migaszewski and Gałuszka 2015; Censi et al. 2017). A recognized example of environmental pollution by REE is that of gadolinium (Gd). For some years now, Gd-based contrast agents have been administered to patients by intravenous injection in order to improve the clarity of magnetic resonance imaging and magnetic resonance angiography scans, as an aid to diagnosis. The dosed Gd is subsequently excreted through the renal system, although there is debate about the proportion of the dose that is retained and can accumulate in the body, e.g., in the brain (Guo et al. 2018; Kanda 2019; Ibrahim et al. 2023). There are reports that such use of gadolinium chelates which are ultimately disposed off through the sewage system results in the contamination of freshwater, drinking water, and beverages that are produced using these waters (Migaszewski and Gałuszka 2016; Schmidt et al. 2019).

Metallic elements and mushrooms

Micro- and macrofungi are key components of forest ecosystems. They recycle chemical elements and other nutrients, often symbiotically benefiting plants, but they are also food for a myriad of organisms including large animals (Lepp et al. 1987; Berendes and Steinhauser 2022). In addition to the physiological necessity of assimilating essential nutrients including minerals from their substrates, macromycetes inadvertently also uptake a variety of environmental pollutants, both inorganic elements, as well as a range of anthropogenic organic chemicals. This uptake and assimilation are well recognized, particularly for potentially toxic elements (PTEs), and has been extensively studied (Falandysz and Borovička 2013; Falandysz 2016; Braeuer et al. 2000; Strumińska-Parulska et al. 2021; Falandysz et al. 2022a; Golovko et al. 2022, and many others). Consequently, the contents of some elements such as Hg, Pb, Cd, or radiocaesium in mushrooms are regulated in some countries and regions.

The potential of mushrooms for mycelial uptake (and temporal storage), transfer, and accumulation of a given chemical element or compound in the fruiting body is estimated using the concept of the bioconcentration factor (BCF) (Tyler 1980). The BCF is the concentration ratio (quotient) of fruiting body occurrence relative to that of the substrate. It can be estimated using the absolute (total) element concentration in the fruiting body. For soil substrates, some estimations use absolute (or pseudo-total) concentrations but also other (extractable-labile, mobile, or adsorbed fraction) concentration data (Grawunder and Gube 2018; Lipka et al. 2018). BCF values for La and Ce for both wild and farmed mushrooms show bio-exclusion (i.e., the BCF ratio is < 1) (Aruguete et al. 1998; Grawunder and Gube 2018; Koutrotsios et al. 2018; Vukojević et al. 2019; Zocher et al. 2018; Mędyk and Falandysz 2022).

Ce, La, and ΣREE in forest soils and wood substrates

Natural concentrations and distribution patterns

Cerium was the most abundant REE in forest topsoils that were collected along with mushrooms in Poland/Belarus, Serbia, and Germany contributing 40–44, 33–38, and 42%, respectively to the sum. La was also abundant, contributing 19–21, 22–22, and 20%, respectively contrasting strongly with lutetium, the least abundant REE with contributions of 0.27–0.46, 0.07–0.08, and 0.30%, respectively (Zocher et al. 2018; Vukojević et al. 2019; Mędyk and Falandysz 2022). The occurrence pattern of REE in the soil is reflected in mushrooms, trees, plants, and other food products (a consequence of the Oddo-Harkins’ order of elemental occurrence), thus maintaining the original abundance patterns (Figs. 1, 2, and 3). Absolute concentrations of REE in foods range from low to ultra-low levels, e.g., based on 79, 91, and 65 positive results (that were above the method quantification limit) out of 98 samples of brown rice, dry weight (dw) concentrations of Ce, La, and Lu were 1.3 µg kg−1, 0.74 µg kg−1, and 0.17 µg kg−1 dw, respectively (Fig. 3). Similarly, respective Ce, La, and Lu concentrations were 7.97, 7.49, and 0.04 µg kg−1 dw in Italian tomatoes, 2.2, 1.3, and 0.085 µg kg−1 fw (fresh weight) in Graviera (Gruyère) cheese from Macedonia, and 13, 2.6, and 0.43 µg kg−1 fw in the muscle meat of wild European rabbits Oryctolagus cuniculus from Greece (Fig. 3). This preserved occurrence pattern owes much to the similarity of the physico-chemical properties between REE, i.e., they all show similar electronic configurations, ionic radii, and a dominant trivalent oxidation state. Consequently, they also have generally, the same biogeochemical fate—they behave similarly or largely as “one element” as they migrate through food webs (Kabata-Pendias and Pendias 1999). A few REE, e.g., Eu and Ce in part can occur also in other oxidation states in the environment which may sometimes lead to an anomaly in their “shale or chondrite normalized” distribution pattern in environmental media (Migaszewski and Gałuszka 2015; Kwecko 2016). Such an anomaly in the occurrence of Eu in mushrooms has been observed by Borovička et al. (2011) as well as in Macrolepiota procera (Falandysz et al. 2017). Similarly, minor anomalies of Eu occurrence were observed for some morphological parts but not for all mushroom samples in another study (Mędyk and Falandysz 2022), or for Suillus luteus which showed a positive anomaly for Y (Zocher et al. 2018). Plots of natural normal- and log-normal distribution of REE occurrence in abiotic and biological samples display the characteristic saw-tooth pattern reflecting the mentioned Oddo-Harkins order. This characteristic is very useful for objective (internal or external) assessment and verification of the credibility and analytical quality of a data set. It is therefore important, scientifically justified, and sound to provide the results of determination of a full range of REEs in the tested matrix, instead of only one or a few randomly selected REE, which is sometimes observed in reported data on mushrooms (Table 1).

Fig. 1
figure 1

Natural normal- and log-normal distribution pattern of lanthanides in annual rings of pine (Pinus massoniana) growing in a REE mining area in China (A), substrates for farmed mushrooms (pine needle, corn combs and data palm tree leaves in Greece; (B) and forest topsoil from Kostryca in Belarus (C) (after Mędyk and Falandysz 2022; Koutrotsios et al. 2018 and Zhang et al. 2019, respectively)

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Fig. 2
figure 2

Natural normal- and log-normal distribution pattern of lanthanides in forest topsoils from Serbia (XS), Germany (G), and Poland (PL) and in wild mushrooms (caps, stems, or whole) from Serbia, Germany, and Poland (after Mędyk and Falandysz 2022; Vukojević et al. 2019 and Zocher et al. 2018, respectively)

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Fig. 3
figure 3

Natural normal- and log-normal distribution pattern of lanthanides in brown rice, tomatoes, pumpkin seeds, cheese, and muscle meat (after Danezis et al. 2017 and 2018; Joebstl et al. 2010; Spalla et al. 2009 and Tagami et al. 2018, respectively)

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Table 1 La, Ce, and ΣREE in macromycetes (µg kg−1 dw; adapted; uncertain or clearly biased data are shown in bold, and with a question mark)
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Biologically, REE are considered to behave similarly to the macroelement, calcium (Ca2+) (Liu et al. 2012; Lange and Peiter 2020). In alcohol dehydrogenase of methylotrophic bacteria, REE can take the place of Ca2+, particularly in the case of those REE that are more abundant in nature such as La, Ce, Pr, and Nd (Pol et al. 2014; Hibi et al. 2011). In addition to this similarity in behavior to the Ca ion, analogies have also been made with the biological coordination chemistry between REE and Fe3+ and Mg2+ (Brown et al. 1990; Guo et al. 2016; Cotruvo 2019). Calcium is one of the main macro-minerals and is present in a large excess in relation to the summed REE concentration in foods, including edible mushrooms (Mędyk et al. 2023). On the other hand, Ca also shares behavioral similarities (Saniewski et al. 2016), with barium (Ba) and strontium (Sr), which like Ca are group II alkaline earth metals. Ca, Ba, and Sr significantly exceed the occurrence of REE in mushrooms. For example, in Suillus grevillei commonly known as the Larch Bolete or Greville’s bolete, the Ca concentration in caps ranged from 80 to 420 mg kg−1 dw, with 220 to 510 mg kg−1 dw in the stems (median values for 6 sample sets with 78 specimens), Ba ranged from 0.89 to 7.1 and 1.6 to 7.7 mg kg−1 dw, and Sr ranged from 0.31 to 1.8 and 0.79 to 2.3 mg kg−1 dw, respectively (Chudzyński and Falandysz 2008). Summed 13–14 REE concentrations in another set of S. grevillei were 0.068 mg kg−1 dw in the caps and 0.049 mg kg−1 dw in the stems (corrected values) (Mędyk and Falandysz 2022). However, possible associations in the occurrence and relationships between REE, Ca, Ba, and Sr in the light of food toxicology are as yet, largely unexplored.

In China, specifically, the REE (largely “a mixture with La, Ce, Nd, and Pr accounting for the main components”) have been used for decades as fertilizers for crops (largely to overcome deficiency symptoms of Ca), and due to overdosing over time, adverse effects have been seen in plants (Redling 2006; Tommasi et al. 2021; He et al. 2022). There is no factual data on whether REE were used in the farming of mushrooms. Farmed mushrooms are largely raised on plant substrates (sawdust, straw, wood, vegetable wastes, etc.), and for some species, additional nutrition can be supplemented through the use of compost like manure (derived from horses and chickens), peat, chalk, and others, but there are no reports of the use of REE (Bhatia et al. 2013; Koutrotsios et al. 2018; Pankavec et al. 2021). REE have been used to promote the growth of livestock but as in the case of crops, it is doubtful if they play any “positive” role (Redling 2006; Schwabe et al. 2012; Tariq et al. 2020).

Artifacts

Sampling artifacts—incrusted sand crystals, adhered soil dust, and herbaria samples

Even very minor contamination of mushroom samples with sand (soil dust) debris will result in elevated concentrations of La, Ce, and other REE and also Al, Ca, Co, Cr, Fe, Li, Ni, Sc, Sr, Th, Ti, V, and Y, as has been documented and explained in the literature (Cocchi et al. 2002; Stijve et al. 2001, 2002,  2004). It is difficult to exclude soil dust from fungal samples taken from sandy soil stands and from truffles simply by using dry clean-up methods, and wet clean-up methods, e.g., rinsing with distilled water, can affect water-soluble potassium and phosphates (Stijve et al. 2004). A stipe (stem, stalk) but also a cap (pileus) of some species can, hypothetically, be incrusted with sand (or soil dust), which in practice is impossible to remove completely. Stijve et al. (2004) found artificially high levels of REE and some of the above-listed elements in species such as Gyrophragmium dunalii (Fr.) Zeller (current name Agaricus aridicola Geml, Geiser, and Royse ex Mateos, J. Morales, J.A. Muñoz, Rey, and C. Tovar (the sand mushroom), Helvella monachella (Scop.) Fr., Morchella dunensis ((current name Morchella esculenta (L.) Pers., (common morel, morel, yellow morel, true morel, morel mushroom, or sponge morel)), Podaxis pistillaris (L.) Fr. (the desert shaggy mane), Psathyrella ammophila (Durieu and Lév.) P.D. Orton (the dune brittlestem) because of incorporated soil dust. Gyroporus cyanescens (Bull.) Quél.) (bluing bolete or cornflower bolete), and other members of the genus Gyroporus (Gyroporaceae) which grow in sandy soils need particular attention if collected (although most are protected species). Also, the popular Tricholoma flavovirens (L.) P. Kumm.—current name T. equestre (L.) P. Kumm., (man on horseback or yellow knight), if collected from sandy soil stands would require particular care during cleaning as would many other sand-dwelling species. Mushrooms growing on wood or plant substrates either wild or farmed would generally be free of dust contamination after cutting out the bottom part of the stipe.

Dried mushrooms if bought from retail outlets can be contaminated by soil dust. Karkocha and Młodecki, who studied the nutritive value of dried Boletus edulis, Agaricus bisporus, Cantharellus cibarius, and Gyromitra esculenta found that the content of sand in these mushrooms (possibly commercial consignments) ranged from 0.55 to 1.8% (Karkocha and Młodecki 1965). Precaution is advised when working with fungal materials deposited in academic herbaria that can be contaminated with soil substrate residues (Borovička et al. 2011). REE data on mushrooms and their substrates can also be affected by analytical chemistry methodologies that are used for determination.

Analytical artifacts

Some analytical methodologies and instrumentation that are used in the determination of REE in biological materials can lead to questionable results for REE, including both La and Ce (Table 1). Measurement by X-ray fluorescence analysis (XRF)—a modern non-destructive technique which has been used in the determination of REE in mushrooms has been highlighted as producing unreliable quantitation in part due to the inadequacy of the method quantitation limits (Borovička et al. 2011; Falandysz and Fernandes 2023). Hence, data obtained using XRF were not included in Table 1. A similar non-destructive technique, neutron activation analysis (INAA), allows the determination of many elements in a sample without matrix decomposition, but in the case of REE, INAA has inadequate instrumental and methodological detection and quantification (LOD, LOQ, MDL, MQL) capabilities for a range of REE. Apart from Ce, Nd, and La, other elements with much lower biological occurrence usually fall below the detection or quantitation limits required for mushroom analysis. Using INAA, Řanda and Kučera (2004) were able to provide results only for La (as well as Sc and a few data for Y). Other practical considerations in using INAA are the poor accessibility, high level of technical and safety training, and the high cost of using the technique.

Inductively coupled-emission/optical mass spectroscopy (ICP-A/OES-MS) which has popularly been used for elemental determination is poorly suited for elements at trace or ultra-trace levels including REE in biological materials because of a combination of insufficient instrumental detection limits, background noise, and spectral interferences, particularly during direct analysis of digested sample extracts (Bulska and Ruszczyńska 2017). Due to these limitations, the use of ICP-OES for the determination of REE in mushrooms or other materials (wood, trees, soil, etc.) was found to yield unreliable results (as commented by Zocher et al. 2018; Falandysz 2022a; Falandysz 2022c). Accordingly, only a small subset of the published literature data on La, Ce, and ΣREE in mushrooms using ICP-OES has been included in Table 1, mainly for comparative and illustrative purposes. ICP, coupled to quadrupole mass spectrometry (ICP-MS) with a collision cell, was used in a few studies to determine REE in mushrooms and their substrates. In these studies, the acid-decomposed sample solution was aspirated directly into the plasma (without any further separation from interferences) which resulted in data that were anomalous from the point of view of analytical chemistry and biogeochemistry, i.e., REE results showed random distribution patterns, and many elements had atypically elevated concentrations. So, in common with the ICP-OES data, apart from a few comparative examples, most of these data were not included in Table 1. These issues on the reliability of REE data based on the analytical methodology used have been discussed in more details in other articles (Zocher et al. 2018; Falandysz 2023b; Falandysz and Fernandes 2023; Falandysz et al. 2024).

The credible determination of REE relies on instrumental techniques that are often expensive or use additional purification steps, but other important aspects include the competence and experience of the analytical chemists. For example, sound knowledge of analytical chemistry, geochemistry, environmental and food science, and knowledge of REE occurrence through the literature as well as through the understanding of necessary laboratory infrastructure, which may seem trivial and mundane are still pertinent issues in 2023.

Patterns—normal and log-normal or shale (or other matrix) normalized and concentration quotients (ratios)

An illustration of the dominance of Ce and La (also Nd) in summed REE occurrence in mushrooms can be observed from the distribution patterns plotted for randomly selected examples in the literature. These are available for farmed and wild epigeous (fruiting above the ground—both ectomycorrhizal and saprotrophic) and hypogeous (below ground) mushrooms, which were obtained using analytical methods with adequate analytical quality and control (AQ/AC) (Fig. 4). Both, relative concentrations and mutual relationships in REE occurrence in mushrooms, their substrates, and some foodstuffs can be explained by the Oddo-Harkins order of elemental occurrence (including REE) as clearly observed by the typical patterns seen in the plotted data in Figs. 1, 2, 3, and 4.

Fig. 4
figure 4

Natural normal- and log-normal distribution pattern of lanthanides in farmed (C. cylindracea and P. ostreatus) and wild mushrooms; whole saprotrophic and ectomycorrhizal species, caps of S. grevillei and in truffle (T. magnatum) (after Borovička et al. 2011; Koutrotsios et al. 2018; Mędyk and Falandysz 2022, and Segelke et al. 2020, respectively)

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Farmed Cyclocybe cylindracea (C. c.) and Pleurotus ostreatus (P. o.) raised on seven plant substrates with natural but different concentrations of La, Ce, and other REE (Koutrotsios et al. 2018) showed BCFs in the ranges: 0.43 to 0.0065 (C. c.), 0.56 to 0.0084 (P. o.), 1.5 to 0.031 (C. c.), and 1.5 to 0.039 (P. o.), respectively. The BCF values of Ce calculated for various morphological parts (pileus trama—flesh of a cap, pileipellis—skin of a cap, lamellae—lamella/gills, stipes—stipe/stem) of Lactarius pubescens ranged from 0.014 to 0.0007 (total), 0.22 to 0.011 (mobile), and 2.4 to 0.12 (adsorbed) (Grawunder and Gube 2018). The BCFs of La and Ce available to date for wild and farmed mushrooms (calculated or cited from literature data) and collated in Table 2, generally show bio-exclusion.

Table 2 The BCFs of La and Ce available to date, for wild and cultivated mushrooms
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These BCFs for Ce and La are in the range of values calculated for Ca in various mushrooms from different collection sites (Jarzyńska et al. 2012; Lipka et al. 2018). Based on the so-called mobile fraction of Ca in the soil substrate which is a portion of the total concentration, BCF values can be greater than 1 (as seen in the above listing for some La and Ce data or for compounds of other elements, largely oxides, which are poorly soluble in pore water). The mycelial network of mushrooms that colonize soil and plant substrates uptake available inorganic compounds readily from the soil solution but also actively search for nutrients originating from rock and mineral bioweathering by excreting chelating agents (Gadd 2017). Mushrooms are much better at bioconcentrating some essential elements like K, Mg, Zn, and Cu (BCF > 1) than La and Ce (and other REE and also Ca, Ba, and Sr) (Jarzyńska et al. 2012; Andersson et al. 2018; Lipka et al. 2018). Toxic elements such as Ag, As, Cd, or Hg occurring at natural concentrations in forest topsoils that are largely similar (Cd) or lower (Ag, As, Hg) than those of Ce or La are much better bioconcentrated (BCF > 1) than REE by mushrooms (Falandysz et al. 2003; Jarzyńska et al. 2012; Árvay et al. 2017; Andersson et al. 2018; Grawunder and Gube 2018; Zhang et al. 2020).

In view of the natural distribution pattern of REE in mushrooms or other biological materials, the values of quotients (concentration ratios) for a given pair of REE should occur within a narrow range regardless of the matrix and type of input data—absolute or shale/chondrite normalized (Falandysz 2023a, 2023c; Falandysz et al. 2024). The La/Ce quotients calculated from available data for certain mushrooms (presented in Table 3) show a narrow range from 0.4 to 0.6, although this may be exceeded in a few examples. Similarly, the La/Ce quotients calculated for shales (Post-Archean Australian Shale, North American Shale Composite, European Shale, and World Shale) that were quoted by Bau et al. were as follows: 0.48–0.51, 0.44–0.47, 0.49–0.51, and 0.49, respectively (Bau et al. 2018). Forest topsoil (0–10 to 0–15 cm layers) at the sites of mushroom collection from Poland showed a La/Ce quotient range from 0.44 to 0.50; the quotient for those collected in Belarus was 0.45 (Mędyk and Falandysz 2022). In three other studies on European mushrooms and soils (Grawunder and Gube 2018; Zocher et al. 2018; Vukojević et al. 2019), the La/Ce quotients for forest topsoil were 0.47 (Ronneburg soil), 0.47 (Jena soil), 0.47 to 0.49 in forested land in Bremen in Germany, and 0.60 to 0.65 in Serbia. In Japanese forests, La/Ce quotients of 0.50 and 0.71 were reported for the litter, fermentation/humifying, and mineral layers of soils, while the ratios were 0.48 and 0.49–0.37 in Sand-dune Regosol and 0.48–0.38 for Andosol (Yoshida and Muramatsu 1997).

Table 3 The La/Ce quotients (ratios) for whole fruiting bodies and their morphological parts of several species
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La and Ce database for mushrooms

An attempt has been made to create a database on the occurrence of La and Ce in mushrooms, both wild and farmed, based on reported literature data. Such a database relies on good-quality data and can be used to establish baseline concentrations for guidance as well as to estimate any future occurrence trends. La and Ce, and summed REE concentration levels, obtained from validated studies (as well as other data with patterns that do not follow the Oddo-Harkins order) were collated (Table 1). Uncertain or clearly biased data as described (Falandysz 2022a, b; 43,44,45,46,47,f; Falandysz et al. 2024) are queried in bold and with a question mark (?). Based on the data in Table 1, the simplified distribution of La and Ce (and summed REE) concentrations in mushroom species collected in Europe is presented in Fig. 5. Concentrations that appear overestimated are shown in red and originate from ICP-OES and/or some ICP-Quad-MS measurements.

Fig. 5
figure 5

The distribution of La, Ce, and ∑REE in mushroom species (as per Table 1) collected in Europe. Concentrations that appear overestimated are shown in red and originate from ICP-OES and/or some ICP-Quad-MS measurements

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Low BCF values and the bio-exclusion of Ce, La, and ∑REE in fruiting bodies suggest that macromycetes are unsuitable for mycomining or the bioremediation of REE, although these occur over a range of concentrations depending on where (above or below the soil or humus substrate), they produce fruiting bodies (Table 1). Two independent studies determined Ce, La, and summed REE in truffles (genus Tuber, species T. aestivum and T. indicum) that produce subterranean fruiting bodies and reported high concentration in the peridium (a thin outer skin membrane covering the fruitbody) with Ce at 2100–4000 µg kg−1 dw and La at 520–910 µg kg−1 dw (the quoted uncertainty was very high, i.e. > 100%), while the gleba (the inner fleshy part) concentrations were substantially lower, i.e., Ce at 73–140 µg kg−1 dw and La at 34–79 µg kg−1 dw (Table 1). The values for gleba were within the range of results reported in wild epigeous fruiting bodies of many species listed in Table 1.

One study reported Ce and La in Pseudohydnum gelatinosum (toothed jelly fungus) at concentrations of 340 and 170 µg kg−1 dw, respectively, maintaining the biogeochemically sound value of the La/Ce quotient at 0.50 (Table 1). The Ca concentration was 240 mg kg−1 dw (Du et al. 2010), which is similar to that cited earlier for Suillus grevillei. In order to maintain body structure, the jelly-like plasmodium of the slime mold Fuligo septica (Myxomycetes, commonly called the dog vomit slime mold or the scrambled egg mold is rich in Ca (8.76% dw, range 4.80 to11.2% dw) chemically close Ba (2550 mg kg−1 dw, range 294 to 15,190 mg kg−1 dw) and Sr (1290 mg kg−1 dw, range 237 to 2190 mg kg−1 dw) (Stijve and Andrey 1999). Hypothetically, this very high content of Ca in parallel to Ba and Sr in F. septica (and potentially in other jelly fungi with elevated Ca) may imply a potential to accumulate the chemically similar REE, but currently, there are no published studies in support of this hypothesis.

La and Ce and ∑REE possible intake and risk through mushroom consumption

Precise data on mushroom consumption in different countries is generally unavailable and likely to be an approximation, if available, as this would be based on the production and sale of cultivated species. This is particularly true for areas where foraging of wild mushrooms is widely practiced. Consumption will also vary depending on personal tastes, growing conditions, and the abundance of particular species. Additionally, estimating dietary intake of contaminants or some nutrients from mushroom meals is difficult especially as mushrooms are very rarely eaten raw (fresh, untreated—as a delicacy) as in the case of Tricholoma matsutake. Household/culinary (or industrial for both farmed and wild species) processing such as blanching, boiling, blanching, and pickling, typically causes pronounced changes (usually a decrease) in the mineral and trace element concentrations of mushrooms (based on whole-weight, meal weight, or wet weight), depending on the species, the process, and the element (Svoboda et al. 2002; Drewnowska et al. 2017a and 2017b; Falandysz et al. 2019; Pankavec et al. 2019 and 2022). Other cooking methods such as frying, braising, grilling, and sometimes also pickling can lead to a small loss or even a slight concentration increase of an element in a mushroom meal compared to the raw product (on a whole/wet weight basis) (Manzi et al. 2004; Daillant et al. 2013; Falandysz et al. 2022a, 2022b and 2022d; Saba 2021). Further uncertainty in estimating dietary intake arises after consumption because gastrointestinal digestion and bioavailability of metallic elements from a mushroom meal are reported to be limited (Pankavec et al. 2023).

It has been reported that some of the local population in the Yunnan (populated with 46.9 million people in 2022) province of China may consume up to 20–24 kg of wild mushrooms (raw product/fresh weight) per capita, annually (Zhang et al. 2010). An older study suggested that individuals in the UK could consume up to 26 kg (Barnett et al. 1999), which could be considered extreme. However, even if an extreme level of consumption is considered (e.g., 30 kg per individual per annum), the low occurrence levels of Ce and La, and ∑REE in unprocessed mushrooms, combined with the effects of culinary processing and limited gastrointestinal digestion and bioavailability (and thus bioaccessibility), would suggest very limited uptake. Thus, based on the current state of knowledge, there is no evidence of a human health risk through mushroom consumption, or from combined (including other foodstuffs and drinking water) exposure. Clearly, this view could change with new knowledge and insights into the toxicology of these elements, both collectively (the effects of mixtures) and individually, and also if there were concurrent increases in the REE occurrence levels in popular species. Given the expanding use of REE globally, such increases cannot be ruled out, and it would be prudent to initiate surveillance not only in edible mushrooms but also in other foods.

Conclusions

The occurrences of Ce, La, and summed REE that have been reported in the literature were assessed through the criteria of environmental geochemistry, analytical chemistry, food toxicology, mushroom systematics, and ecology. Based on the type of instrumentation used for measurement and the quality of the analytics used for determination, some data were excluded, particularly when the collective REE occurrence patterns deviated from those predicted by the Odo-Harkins order. The collated data shows that Ce and La accumulate similarly in fruiting bodies and are not fractionated during uptake, maintaining the original occurrence patterns of the substrates in which the fungi grew. There is also no credible evidence that the other REE undergo variable uptake because the evaluated data show natural, unfractionated patterns in accordance with the Oddo-Harkins’ order of environmental lanthanide occurrence. Ce and La were the first and the third most abundant lanthanides in wild and farmed mushrooms regardless of substrate, with Ce occurrence approximately double that of La. The species covered in this report also appear to bio-exclude REE. The fruit body concentrations were two to four orders of magnitude lower than the growing substrates (where reported). This is corroborated by the low values (ranging from 0.001 to below 1) of independently reported bioconcentration factors. There is scant information on the toxicological implications of dietary intake of REE, but the current state of knowledge provides no evidence that wild or cultivated mushrooms pose a health risk either by themselves or when included with the rest of the diet. However, given the growing and varied use of REE in commercial applications, it would be prudent to monitor REE concentrations in environmental and food-related matrices in the future.