2022 年 28 巻 4 号 p. 297-306
The six heavy-metals and ten minerals in ten wood-rotting mushrooms were determined. Pb was not detected. Cd (0.02–0.32 mg/kg), Hg (0–0.05 mg/kg), and As (0.04–0.82 mg/kg) did not exceed Chinese standard levels, except for the Hg (2.15 mg/kg) in one Oudemansiella raphanipes sample. Auricularia heimuer had high levels of Ca (11 209 mg/kg) and Fe (603.54 mg/kg), indicating its suitability as a functional food. O. raphanipes with high contents of Fe (192.66–682.62 mg/kg), Zn (88.11–107.17 mg/kg), and K (17 273–22 560 mg/kg), which can be used as health food to supplement Fe, Zn, and K simultaneously. Pleurotus citrinopileatus was rich in Se (0.11–0.47 mg/kg) and it can be used as a Se-rich supplement (0.1–10 mg/kg). Ca and Mg, P and K, and K and Mg were highly and significantly positively correlated, indicating that they could co-accumulate in the mushrooms.
Fe, Zn, Cu, Mn, and Se are essential trace elements, whereas Ca, P, K, Mg, and S are essential major elements indispensable to the human body (Andy, 2019). A deficiency of these elements can cause several diseases. For example, about one-third of the global population suffers from anemia, among whom, the majority suffer from Fe deficiency (Auerbach and Adamson, 2016). Thus, Fe supplementation is vital to prevent anemia. Among the inorganic elements in the human body, Ca accounts for a maximum of up to 2% of the total body weight (Theobald, 2005). The daily recommended intake of Ca in adults is 1 000–1 200 mg. Ca deficiency can lead to osteoporosis and fractures (Coy et al., 2020). Zn is required for essential functions at the biological and molecular levels, as it serves as a prosthetic group for enzyme catalysis or a cofactor in several metabolic reactions (Ozeki et al., 2020). As long as an individual consumes a normal diet, there will be no zinc deficiency. Zn deficiency is observed in chronic malnourishment and individuals following a vegetarian diet. Zinc deficiency predisposes individuals to liver disease and results in stunted growth in children (Ozeki et al., 2020; Wessells and Brown, 2012). K is an essential nutrient for human growth and the most abundant cation in the body. A lack of K could lead to arrhythmia, as often seen in a clinical setting (Theisen-Toupal, 2015). Moreover, muscle weakness (Chhabria et al., 2020) and hemiplegia (Chidi and Peter, 2010) are common outcomes of K deficiency, and in severe cases, respiratory failure (Naji and Her, 2018), cardiac arrest (Martindale et al., 2014), and even death (Mattsson et al., 2018) may occur. Se is an important component of many selenium amino acids and selenium proteins that plays a role in several biochemical reactions in animals and humans (Birringer et al., 2002; Tapiero et al., 2003). Se can prevent cancers, reduce the incidence of viral infections, prevent cardiovascular diseases and arthritis, and improve immunity (Puccinelli et al., 2017; Tapiero et al., 2003). Supplementation of food with minerals is a simple and effective process to ensure a balanced diet. With an improvement in living standards, there has been a change in lifestyle choices, and several people now opt to voluntarily incorporate health foods into their diet. For example, peas are a rich source of Fe, Zn, and Mg (Amarakoon, et al., 2012), whereas maize -bambara groundnut can be used to supplement Ca, Fe, Zn, and vitamin A (Uvere et al., 2010). Foods made from potato, soybean, and carrot powder can be used to fortify the diets of infants and children with vitamin A, Fe, Zn, and proteins (Adetola et al., 2020).
Compared with plant foods, edible and medicinal mushrooms can better accumulate specific minerals (Przemysław et al., 2017). Several elements have been found to be present in mushrooms at significantly high levels. Therefore, mushrooms are not only a good source of high-quality proteins but are also a valuable food source in providing the body with essential minerals (Krittanawong et al., 2020). For instance, the levels of K (38 105–39 566 mg/kg) and P (10 430–11 235 mg/kg) in Agaricus bisporus (Tsukuritake) (Vetter, 2003) and Zn (28 570 mg/kg) in Cordyceps militaris (Sanagitake) (Cheng et al., 2010) are extremely high; therefore, these mushrooms can be used to supplement foods with K, P, and Zn. The Grifola frondosa (Maitake) can accumulate seven minerals (Ca, Cu, Fe, Mg, Mn, P, and Zn) (Przemysław et al., 2017); Boletus (Iguchi) species can accumulate six minerals (P, K, Fe, Mg, Ca, and Na) (Wang et al., 2015), and Tricholoma matsutake (Matsutake) can accumulate four minerals (K, Na, Ca, and Mg) (Tschudy and Watson, 2013). These edible and medicinal mushrooms can also be used as health foods to obtain the collective daily dose of minerals. Hericium erinaceus (Yamabushitake) is used as a dietary source of bioavailable Se (Ting et al., 2020). In addition to being a rich source of minerals, edible and medicinal mushrooms are health foods that are low in fat and have low calorific values (Przemysław et al., 2017). Moreover, these mushrooms are readily available as their cultivation techniques have been mastered.
Recent studies on the accumulation of heavy metals in edible and medicinal mushrooms have been a cause of concern (Chungu et al., 2019). Wang determined the heavy metal content in eight wild edible mushrooms available in the Chinese markets, and found high levels of Co, Mn, Ni, and Fe (Wang et al., 2017). Li discovered that Panus giganteus could hyperaccumulate Pd (Li et al., 2011; Liu et al. (2015). conducted a study to determine the heavy metal content in several wild edible mushrooms in the Yunnan Province. They reported that the levels of essential elements required by humans were within the normal range; however, the levels of heavy metals in the mushrooms exceeded the prescribed standards, thereby being a potential source of toxicity (Liu et al., 2015; Kokkoris et al., 2019). determined the levels of Cr, Cu, Fe, Mn, Ni, Pb, and Zn in six wild edible mushrooms in the Athens area and found that among the five heavy metals in the samples, Pb content exceeded the permissible levels. Therefore, close attention should be paid to the heavy metal content during the cultivation of edible and medicinal mushrooms.
In this study, using apple sawdust as the main material and a suitable formula, the 10 wood-rotting edible and medicinal mushrooms were cultivated. The fruit body of each mushroom variant was treated using the microwave digestion method. The heavy-metal and mineral content were determined using inductively coupled plasma optical emission spectrometry (ICP) (Sarikurkcu et al., 2012). In this study, we determined the levels of heavy metals and minerals elements in various medicinal and edible mushrooms. Moreover, we attempted to identify the mushrooms in which beneficial elements could be enriched without simultaneously increasing the levels of the harmful elements.
Materials and Media The mycelia of Pleurotus ostreatus (Jacq.) Quél. (Hiratake), Pleurotus citrinopileatus Singer (Tamogitake), Pleurotus cornucopiae (Paulet) Quél. (Tamogitake), Ganoderma lingzhi Sheng H. Wu, Y. Cao & Y.C. Dai (Mannentake), Pleurotus pulmonarius (Fr.) Quél. (Usuhiratake), Flammulina velutipes (Curtis) Singer (Enokitake), Oudemansiella raphanipes (Berk.) Pegler & T.W.K. Young, Pleurotus giganteus (Berk.) Karun. & K.D. Hyde, Lentinula edodes (Berk.) Pegler (Shiitake), and Auricularia heimuer F. Wu, B.K. Cui & Y.C. Dai (Kurokiku rage) were provided by the Key Laboratory of Edible Fungus Technology of College of Agriculture, Ludong University (all these samples are cultivars).
In addition to the sawdust obtained from homegrown apple trees (processed by Qixia applewood in Base I; Laboratory of Ludong University), other cultivation materials, including apple sawdust, corn cob, cottonseed husk, and bran, were purchased from suppliers.
Preparation of culture medium for the first isolated generation: formulation of solid potato dextrose agar (PDA) medium: potato (peeled) 200 g, glucose 20 g, peptone 20 g, agar 20 g, water 1 000 mL; pH was not adjusted. To prepare liquid PDA medium, the same formulation indicated to prepare the solid PDA medium was used, with the omission of agar.
Preparation of the culture medium for the second generation: fresh wheat 96%, bran 2%, gypsum 2%.
The culture medium of the third generation including the cultivation formulae for the edible and medicinal mushrooms, is displayed in the Results section (Table 1).
| Test base | Species | Formula |
|---|---|---|
| I | P. ostreatus, P. citrinopileatus, P. cornucopiae, P. pulmonarius G. lingzhi, F. velutipes O. raphanipes | apple sawdust 50%, cottonseed husk 20%, corn cob 20%, wheat bran 8%, gypsum 2%; water content: 60% |
| II | P. ostreatus | apple sawdust 25%, corn cob 53%, wheat bran 20%, gypsum 2%; water content: 60% |
| P. citrinopileatus | apple sawdust 68%, corn cob10%, wheat bran 20%, gypsum 2%; water content: 60% | |
| O. raphanipes P. giganteus | apple sawdust 54%, corn cob 24%, wheat bran 20%, gypsum 2%; water content: 60% | |
| III | L. edodes | apple sawdust 81%, wheat bran18%, gypsum 1%, CaO 0.3%; water content: 57% |
| IV | A. heimuer | apple sawdust 98%, gypsum 2%; water content: 60% |
Note: I: Shandong Key Laboratory of Edible Mushroom Technology; II: Yantai Fuai Huinong Rare Edible Mushroom Development Co. Ltd (Yantai, China); III: Qingdao Hua Sheng Quan Biotechnology Co., Ltd (Qingdao, China); IV: Yantai Hexian Modern Agricultural Technology Co., Ltd (Yantai, China). In addition to base 1 apple wood, the materials for the cultivation mushrooms were all purchased from Qixia Xurui Biological Technology Co., Ltd (Yantai, China). The apple wood, corncob and bran of bases II and III are from the same batch, and other raw materials are from different batches.
Reagents The main reagents used for experiments were ethanol (75%), concentrated nitric acid (analytical purity, superior purity), millipore water, etc.
Strain Preparation The first isolated generation was prepared from preserved strains, which were inoculated on solid PDA on an inclined plane and cultured at 25 °C for 7–10 days. The inclined plane was covered, and the mycelia of the first isolated generation were inoculated on the culture medium of the second generation. The second generations were cultured in 300 mL glass bottles at 25 °C for about 15 days. The second generation was transferred to a sterile bacteria-free bag to prepare the third generation.
Spawn Production and Growth Applewood and the pruned branches were crushed to yield sawdust. Then, the naturally dried sawdust was transferred to a mixer, water was added, and the contents were submerged and soaked for 8–12 h. The media were prepared in a mixer by filling apple sawdust and nutrient supplements (cottonseed husk, corn cob, wheat bran, gypsum), followed by stirring for 10 min. Next, the substrates were humidified with water to achieve a 55%–65% water content, which was calculated and confirmed after preparation. The substrates were stirred for 30–50 min. The prepared media were packed into polypropylene plastic bags (330 mm × 170 mm × 0.6 mm to a total weight of 1 500 g), and each mushroom variant was divided into three groups with 50 bags per group. The packed media were autoclaved at 121 °C for 2–4 h. After cooling, the second generation was inoculated in a sterile environment. The inoculated culture bags were maintained at 25 °C in a temperature-controlled room. When the culture bags were full of mycelia, they were moved into the growing room or mushroom shed. The management technique of mushroom growth was performed per the management requirements of each variety.
Mode of mushroom production: P. ostreatus, P. citrinopileatus, P. cornucopiae, G. lingzhi, P. pulmonarius, and F. velutipes in base I were cultivated in bags in the growing room; P. ostreatus and P. citrinopileatus in base II and L. edodes in base III were cultivated in bags in the shed. In base I, the mycelia-containing O. raphanipes bag was opened and covered with a layer of soil. O. raphanipes and P. giganteus in base II were cultivated in the shed on beds covered with soil and without the bags. A. heimuer in base IV was cultivated using open-air bag-type fruiting.
Sample collection, Microwave Digestion, and Mineral Detection Fruiting bodies are collected after growing. The fruiting bodies were placed in a Petri dish, exposed to a 60 °C blast-dryer fan, baked to a constant weight, and crushed. A total of 0.2 g of the fruiting-body powder was added to the digestion tube. Next, 6 mL of concentrated HNO3 was added, the cover was opened, and the samples were soaked in the fume cupboard overnight. Then, the samples were placed in a microwave digestion instrument, heated to 130 °C over a 10-min period, incubated at this temperature for 5 min, and then heated to 180 °C over a 10-min period. This temperature was held for 30 min, and then lowered to 60 °C. Next, the digestion tube was opened and placed into an acid discharge meter (140 °C) to discharge the acid. After complete draining, 1 mL of concentrated HNO3 was added to the residue and dissolved, and the volume was made up to 50 mL with pure water. A total of 8–9 mL of the supernatant was placed in a centrifugal tube and the absorbance was measured using a Prodigy full-spectrum direct-read ICP emission spectrometer (Teledyne Leeman Labs, Hudson, NH, USA). The digestion and determination methods of culture materials are the same as described above.
Data Analysis Data were analyzed using Microsoft Excel 2007, SigmaPlot 10.0, SPSS 17.0, and R studio.
Test Base, Species, and Formula With applewood as the main material, 10 edible and medicinal mushrooms were successfully cultivated on waste wood, including P. ostreatus, P. citrinopileatus, P. cornucopiae, G. lingzhi, P. pulmonarius, F. velutipes, O. raphanipes, P. giganteus, L. edodes, and A. heimuer. Details of the species and formulations of the edible and medicinal mushrooms cultivated in the base are shown in Table 1. The same materials and formulae were used to cultivate P. ostreatus, P. citrinopileatus, P. cornucopiae, G. lingzhi, P. pulmonarius, F. velutipes, and O. raphanipes in the laboratory. Other company bases use the best formula to produce corresponding edible and medicinal mushrooms, and these materials were purchased from the respective suppliers.
Determination of Mineral Content in Cultivated Materials The mineral content in the cultivated materials was determined. The content of Cd, Pb, and Hg in apple sawdust in base I were higher (Table 2). The mineral content of the different cultivation materials was found to vary substantially. The level of P in wheat bran was found to be much higher than that in sawdust, cottonseed husk, and corn cob. The levels of K, Mg, S, Mn, and Zn in bran were also found to be relatively high. The Ca levels in sawdust and the Cu and Ni level in corn cob were significantly high. The differences in the mineral levels of the same cultivation material in different bases may be attributed to different producing areas.
| Base I Apple sawdust |
Base II, III Apple sawdust |
Base IV Apple sawdust |
Base I Cotton seed husk |
Base I Corn cob |
Base II, III Corn cob |
Base II, III Wheat bran |
Base IV Wheat bran |
Base I Soil |
Base II Soil |
|
|---|---|---|---|---|---|---|---|---|---|---|
| Ca | 9609µ512b | 16279µ967a | 10334µ1992b | 2684µ517c | 2800µ453c | 2464µ374c | 3088µ535c | 1564µ260c | - | - |
| P | 401µ66b | 922µ205b | 341µ44b | 830µ83b | 1075µ158b | 1140µ254b | 11858µ2672a | 12202µ2099a | - | - |
| K | 3378µ383d | 2921µ317d | 1499µ317e | 8119µ518b | 6288µ298c | 7422µ589b | 11295µ655a | 10447µ1012a | - | - |
| Mg | 1180µ135bcd | 1600µ103bc | 1058µ99cd | 1623µ238b | 683µ106d | 792µ86d | 4409µ350a | 4049µ612a | - | - |
| S | 718µ201d | 1797µ137bc | 1135µ87cd | 1422µ112bcd | 1089µ163cd | 2070µ269b | 4340µ479a | 3801µ827a | - | - |
| Fe | 424.37µ64.60d | 1278.37µ94.80b | 160.98µ29.58e | 156.84µ52.44e | 733.84µ59.85c | 1711.82µ154.25a | 609.90µ101.16c | 331.62µ48.57d | - | - |
| Zn | 40.80µ6.25c | 32.04µ4.02cd | 22.38µ4.63de | 12.14µ1.72e | 36.89µ3.97c | 55.93µ4.36b | 96.20µ10.25a | 94.31µ5.59a | - | - |
| Cu | 63.10µ5.79b | 56.11µ7.23b | 32.39µ4.47c | 28.02µ4.04c | 125.44µ7.73a | 115.84µ19.16a | 27.05µ11.01c | 29.13µ4.10c | - | - |
| Mn | 48.30µ9.77c | 59.66µ5.30c | 77.31µ2.99b | 14.29µ1.85d | 18.59µ1.02d | 56.79µ3.92c | 130.12µ0.63a | 138.86µ11.32a | - | - |
| Se | 0.038µ0.0062a | 0.016µ0.0027d | 0.019µ0.0042cd | 0.044µ0.0041a | ND | 0.028µ0.0042b | 0.028µ0.0032bc | 0.029µ0.0027b | - | - |
| Cr | ND | 4.67µ1.03b | 1.44µ0.21c | ND | 1.99µ0.27c | 11.70µ1.65a | 1.43µ0.24c | 1.42µ0.09c | 55.00µ2.00a | 35.67µ4.04b |
| Ni | 11.89µ1.38d | 19.48µ2.50c | 12.11µ1.70d | 4.79µ1.00e | 69.79µ4.49a | 51.87µ4.46b | 7.29µ0.63de | 9.95µ1.42de | 26.67µ0.58a | 19.00µ2.00b |
| Pb | 2.30µ0.48a | ND | ND | ND | ND | 2.00µ0.37a | ND | ND | 25.33µ0.58a | 24.67µ0.58a |
| Cd | 1.31µ0.18a | 0.07µ0.01b | 0.11µ0.01b | 0.03µ0.01b | ND | ND | 0.04µ0.01b | 0.02µ0.01b | 0.11µ0.02a | 0.11µ0.01a |
| Hg | 0.031µ0.0066a | 0.012µ0.00050bc | 0.0067µ0.0025bc | ND | ND | 0.014µ0.0045b | 0.0053µ0.00086c | ND | 0.093µ0.004a | 0.033µ0.002b |
| As | 0.22µ0.04b | 0.35µ0.04a | 0.13µ0.03d | 0.05µ0.01e | 0.24µ0.04b | 0.20µ0.03bc | 0.31µ0.03a | 0.15µ0.02cd | 10.07µ0.47a | 9.33µ0.35a |
Note: ND: not detected.-: not determined. Detection limits for Se, Cr, Pb, Cd, Hg are 0.01, 0.05, 0.02, 0.002, and 0.001 mg/kg, respectively. Resultsrepresent means of three replicates µ SD. In the same line, same letters mean no significant difference, different letters mean significant difference, P <0.05.
Contents of the Heavy Metals in the Fruiting Bodies Based on the Chinese national standard, GB 2762-2017 National Food Safety Standard–Limits of Contaminants in Food, and the agricultural standard, NY/T 749-2018 Green food Edible Mushroom, the levels of Pb, Cd, and As in the fruiting bodies of edible and medicinal mushrooms were determined. Pb was not detected in any of the mushroom samples. Cd and As levels in the mushroom samples were recorded in the dried form. Cd and As levels in all samples were well within the limits prescribed by the agricultural standard, NY/T 749-2018. Hg levels in the samples did not exceed the standard threshold, except in the case of O. raphanipes (2.15 ± 0.24 mg/kg) in base I (Fig. 1). Hg levels in the O. raphanipes in base II and in other edible and medicinal mushrooms in base I were within the standard levels. The high Hg content in O. raphanipes in base I may be attributed to the covering soil (Table 2).
Heavy metal content in edible and medicinal mushroom samples. 1–8: P. ostreatus, P. citrinopileatus, P. pulmonarius, P. cornucopiae, F. velutipes, O. raphanipes, Caps of G. lingzhi, and Stipes of G. lingzhi in Base I; 9–12: P. ostreatus, P. citrinopileatus, O. raphanipes, and P. giganteus in Base II;13–14: Caps of L. edodes and Stems of L. edodes in Base III; 15: A. heimuer in Base IV. Error bars: results represent means of three replicates ± SD. Same letters mean no significant difference, different letters mean significant difference, P <0.05.
As established reference standards for Cr and Ni threshold in the mushroom samples were unavailable, the Cr (0–18.92 mg/kg, 0–21 mg/kg), Ni (5.9–78.7 mg/kg and 0.43–39.4 mg/kg) levels in wild edible mushrooms (Marek et al., 2017; Sarikurkcu et al., 2012; Wang et al., 2017; Sarikurkcu et al., 2020) were compared with the corresponding levels of Cr (0–9.46 ± 1.06 mg/kg) and Ni (0–24.07 ± 3.36 mg/kg) and found to be low in our study. However, a horizontal comparison showed that Cr levels in F. velutipes cultivated in base I (9.46 ± 1.06 mg/kg) and O. raphanipes in base II (6.33 ± 0.63 mg/kg) were very high, and Ni levels in the stipe of G. lingzhi in base I (24.07 ± 3.36 mg/kg) and O. raphanipes in base II (18.21 ± 2.01 mg/kg) were very high. These findings indicated that mineral levels in mushrooms should be controlled (Fig. 1).
Levels of Major Elements and Trace Elements in the fruit body Ca, K, P, Mg, S, Fe, Zn, Cu, Mn, and Se levels in the cultivated mushroom samples ranged from 23 ± 4–11 209 ± 2 263 mg/kg, 3 153 ± 369–22 847 ± 3 658 mg/kg, 1 602 ± 358–14 041 ± 2 901 mg/kg, 609 ± 81–3 575 ± 282 mg/kg, 3 478 ± 383–17 718 ± 2 048 mg/kg, 28.56 ± 1.92–682.62 ± 43.57 mg/kg, 20.14 ± 3.46–107.17 ± 18.10 mg/kg, 5.07 ± 1.35–88.16 ± 8.76 mg/kg, 4.64 ± 0.88–36.81 ± 4.89 mg/kg, and 0.034 ± 0.0 078–0.47 ± 0.10 mg/kg (Fig. 2), respectively.
Mineral element content in edible and medicinal mushroom samples.1: P. ostreatus in Base I, 2: P. ostreatus in Base II, 3: P. citrinopileatus in Base I, 4: P. citrinopileatus in Base II; 5: O. raphanipes in Base I, 6: O. raphanipes in Base II; 7: Caps of L. edodes grown in Base III; 8: Stems of L. edodes grown in Base III; 9: Caps of G. lingzhi grown in Base I; 10: Stems of G. lingzhi grown in Base I; 11: P. pulmonarius in Base I; 12: P. cornucopiae in Base I; 13: F. velutipes in Base I; 14: P. giganteus in Base II; 15: A.uricularia heimuer in Base IV. Error bar: results represent means of three replicates ± SD. Same letters mean no significant difference, different letters mean significant difference, p < 0.05.
Among the mineral levels in the fruiting bodies of different edible and medicinal mushrooms (P. ostreatus, P. citrinopileatus, P. pulmonarius, P. cornucopiae, F. velutipes, O. raphanipes, G. lingzhi) cultivated using the same source of cultivation materials in base I, the stems of G. lingzhiwere found to accumulate the highest levels of Ca, Fe, Cu, and Mn. P. citrinopileatus showed the highest levels of P, S, Zn, and Se; and F. velutipes was found to accumulate the highest levels of K and Mg (Fig. 3). These finding indicated that the different edible and medicinal mushrooms could selectively accumulate different heavy metals.
Mineral content in the fruiting body of edible and medicinal mushroom in Base I. 1: P. ostreatus; 2: P. citrinopileatus; 3: P. pulmonarius; 4: P. cornucopiae; 5: F. velutipes; 6:O. raphanipes; 7: Caps of G. lingzhi; 8: Stems of G. lingzhi. Error bar: results represent means of three replicates ± SD. Same letters mean no significant difference, different letters mean significant difference, p < 0.05
The same variety of mushrooms propagated in different bases was found to have a similar ability in the accumulation of minerals. For example, the Fe content of O. raphanipes grown in Base II was the highest (682.62 ± 43.57 mg/kg), which was more than three times that grown in Base I (192.66 ± 16.97 mg/kg). However, the Fe content of O. raphanipes grown in Base I still ranked second (Fig. 2, Fig. 3). The Se levels of P. citrinopileatus grown in base I was the highest (0.47 ± 0.10 mg/kg); moreover, Se levels of P. citrinopileatus grown in base II were not low (0.11 ± 0.032 mg/kg) (Fig. 2, Fig. 3). The reason why the levels of the same minerals in a particular variety of mushroom varies can mainly be attributed to the different minerals in the different bases used for cultivation.
Depending on the base used for cultivation, A. heimuer can accumulate Ca, Mg, and Fe; L. edodes can uptake S; O. raphanipes can accumulate Fe and Zn; the stems of G. lingzhi can accumulate Cu; and P. citrinopileatus can take up Se. In this study, A. heimuer was found to have high levels of Ca (11 209 ± 2 263 mg/kg) and Fe (603.54 ± 32.25 mg/kg), indicating its potential in the use as functional and health supplements. High levels of Fe, Zn, and K were found in O. raphanipes ( Fe: 192.66 ± 16.97–682.62 ± 43.57 mg/kg, Zn: 88.11 ± 6.61–107.17 ± 18.10 mg/kg, and K: 17 273 ± 954–22 560 ± 2 434 mg/kg), highlighting the role of this mushroom as functional food in supplementing Fe, Zn and K. The Se content was high in P. citrinopileatus (0.11 ± 0.032–0.47 ± 0.10 mg/kg), which matched the stated requirement of selenium-rich edible and medicinal mushrooms (0.1–10 mg/kg) (DB6124.01-2010) (Fig. 2).
Correlation analysis of Elements in fruiting bodies Correlation analysis of the major and trace elements in the fruiting bodies of mushrooms compared with the levels present in humans showed that only Ca was significantly correlated with Mg and Fe; P was significantly correlated with K and Cu; K was significantly correlated with Mg; Fe was significantly correlated with Cu and Mn; and Cu was significantly correlated with Mn (Fig. 4). The correlation between Ca and Mg, P and K, and K and Mg reached extremely significant levels, indicating that they could co-accumulate in the fruiting bodies of edible and medicinal mushrooms.The correlation between S and other elements was not strong, which may be related to the instability of S in mushrooms rendering it susceptible to easy oxidation and volatilization.
Correlation matrix of major elements and trace elements in sub-entities. Numbers in the circle indicate Pearson correlation coefficients (r) between the corresponding variables (p < 0.05), proportional to the size of the colored dots. Empty cells indicate non-significant correlations (p > 0.05).
With the development in the economy and a growing requirement for quality foods, the sphere of health foods and nutritional supplements is expanding exponentially. As health foods are useful in supplementing and providing trace elements to the body, edible and medicinal mushrooms may appear suitable in this aspect. Mushrooms can be used as a source of various trace elements owing to their wide acceptance and ready availability. The accumulation of the beneficial elements, Fe, Zn, and K, in O. raphanipes, which was screened in this study, has not been reported before. Ca accumulation in A. heimuer (11 209 ± 2 263 mg/kg) was higher than that reported in a previous study (2 590.35–5 318.21 mg/kg) (Liu, 2015). The accumulated Se levels in P. citrinopileatus were lower than those reported in the literature (4.09 mg/kg) (Marek et al., 2017). These results indicated that cultivation materials had a great influence on the accumulation of minerals in the fruiting bodies of edible and medicinal mushrooms. Based on the accumulation characteristics of various elements in edible and medicinal mushrooms, the levels of these enriching and beneficial elements could be successfully manipulated by regulating the element composition of the cultivation and growth substrates.
O. raphanipes is rich in Fe and Zn, whereas A. heimuer is rich in Ca and Fe. The enrichment of these ions in the mushrooms may be related to the coordinated transport of metal cations. ZIP (Korshunova et al., 1999), Nramp (Curie et al., 2000), CDF (Cotrim et al., 2019), and other family genes have been studied in plants for a long time. These homologous genes have also been discovered in edible and medicinal mushrooms and may participate in the transport of divalent cations in organisms. In future studies, the mechanism that leads to the accumulation of mineral elements in edible and medicinal mushrooms should be elucidated. Moreover, the accumulation and uptake of beneficial elements can be further improved based on engineering technology.
Contrary to previous studies wherein the elemental content of wild edible and medicinal mushrooms or the heavy-metal levels of selected cultivated edible mushrooms were determined, in this study, we comprehensively determined the accumulation characteristics of six heavy metals and ten minerals in ten commercially cultivated wood-rotting edible and medicinal mushrooms. However, our study have some deficiencies. We did not elucidate the mechanism of accumulation of minerals in the mushrooms evaluated in this study. The fact that the inter-species difference of mineral element accumulation has not been sufficiently verified. In the future research, we will focus on the accumulation of Ca, Fe, Zn and K in different strains of A. heimuer and O. raphanipes to verify the intra-species differences. . We will add different concentrations of Ca, Fe, Zn, and K to the medium to study whether there is specific accumulation of corresponding elements in A. heimuerand and O. raphanipes and study the accumulation of these elements at the added different concentrations and different developmental stages of the two edible mushrooms. We will also attempt to clarify the accumulation patterns of minerals in fruiting bodies at different developmental stages and under different element concentrations, which will help lay the foundation to further reveal the mechanism of mineral accumulation in edible and medicinal mushrooms.
Acknowledgments This work was supported by the National Natural Science Foundation of China (Nos. 31400447), Key Research and Development Program in Shandong Province (No. 2017NC210006), Major Scientific and Technological Innovation Projects of Key Research and Development Program in Shandong Province (No. 2019JZZY010717), Edible Mushroom Genetic Breeding Innovation Team of Shandong Agricultural Industry Technology System (2016 No.18), and the Project of Shandong Province Higher Educational Science and Technology Program (No. J17KB184).
Conflict of interest There are no conflicts of interest to declare.
