Various Factors on Calcium Enrichment in Edible Mushrooms: History
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Zhen-Xing Tang
,
Lu-E. Shi
,
Zhong-Bao Jiang
,
Xue-Lian Bai
,
Rui-Feng Ying

Calcium is one of the essential minerals that enhances various biological activities, including the regulation of blood pressure, the prevention of osteoporosis and colorectal adenomas. Calcium-enriched edible mushrooms can be considered as one of the important daily sources of calcium in foods. Calcium accumulation in edible mushrooms is an effective way to enhance its activities because the organic state of calcium metabolites in edible mushrooms can be formed from the original inorganic calcium.

  • calcium
  • enrichment
  • edible mushrooms
  • mechanism

1. Introduction

Calcium, one of the important microelements, has been demonstrated to exhibit great advantages to our health [1][2]. Calcium is not only essential for the growth of bones and teeth, but it also takes part in various physiological metabolisms of our body, such as the regulation of muscle contraction, blood coagulation, etc. [3][4][5]. Recently, the literature has offered findings that show the occurrence of various diseases, mainly osteoporosis, cardiovascular, male infertility, etc., is highly correlated to calcium deficiency [6][7][8]. So, the consumption of foods with high calcium levels is highly encouraged [9][10]. The intake of calcium from dairy sources, such as milk, cheese, yogurt, etc., is a commonly recommended way to satisfy the body’s calcium requirement [10][11]. Some non-dairy calcium sources from vegetables, including broccoli, kale, Chinese cabbage, etc., are also suggested [10]. The majority of people realize that calcium is a vital mineral for our health; however, humans are not getting sufficient calcium in their diets, in accordance with the recommendations of many nations and agencies [12][13][14][15]. To satisfy the need for calcium, the intake of calcium from calcium supplements is usually adopted. Many calcium supplements, including CaCl2, CaCO3, calcium gluconate, calcium amino acid chelate and peptide calcium, have been made available, which have played a great role in providing calcium to the human body [16][17]. However, these calcium supplements have some drawbacks, for instance, the low solubility of inorganic calcium, poor absorption and utilization efficiency, etc. [17][18]. Therefore, to meet the calcium requirements, the development of higher-bioavailability, safer and cheaper calcium supplements is rather necessary.
Many beneficial microorganisms such as probiotics, yeasts, edible mushrooms, etc., show great potential for the accumulation of minerals [17][19][20][21]. Among these microorganisms, edible mushrooms can be regarded as an interesting object of supplementation. In numerous countries, edible mushrooms have been part of the daily diet for several thousand years [22][23]. They are regarded as a nutritious food, referring to the many nutritious substances they contain, including polysaccharides, minerals, dietary fibers, proteins, vitamins, etc. [23][24]. Furthermore, owing to their many bioactive characteristics, for example, anti-cancer, anti-bacterial, anti-oxidation, anti-inflammatory, etc., edible mushrooms can also be considered as functional foods with potential advantages for our health [24][25][26][27][28][29]. There are about 100 species that are commercially available in the global mushroom market. Around 20 species have the potential to be cultivated at an industrial level [30][31]. The world outputs of edible mushrooms have increased dynamically year by year, varying from 10.5 million tons in 2016 to 11.8 million tons in 2019, with an increase of around 57% over the last 10 years [32]. It is important to highlight that the worldwide market for edible mushrooms in 2019 was USD 16.9 billion in 2019, whereas it is anticipated to reach USD 19.04 billion by 2026 [33]. China is the largest manufacturer of edible mushrooms in the world, and its production is still on the rise [34][35][36][37].
Owing to edible mushrooms’ excellent capacity to accumulate minerals, numerous studies on minerals enriched in edible mushrooms have been carried out to help improve the nutritive value of edible mushrooms. Edible mushrooms fortified with calcium are extremely interesting, showing great potential as a calcium dietary supplement [38][39][40]. In view of the increasing demand for natural dietary supplements, Ca-fortified edible mushrooms can be regarded as a type of marketable product with great commercial potential. Compared to studies of other enriched minerals such as selenium [41][42][43], the investigations for Ca accumulation in edible mushrooms are relatively limited. The most common calcium enrichment method involves the addition of exogenous calcium salts into a substrate or fermentation medium. Consequently, calcium-fortified edible mushrooms have the potential to be a safe and effective source of daily Ca supplementation, exhibiting the benefits of safety and effectively promoting organic Ca formation [44][45][46].

2. Effects of Various Factors on Calcium Enrichment in Edible Mushrooms

Edible mushrooms are rich in many essential minerals [47][48][49][50][51], including potassium, calcium, phosphorus, and magnesium, which are often deficient in our daily diet [52][53]. Accordingly, the investigation of Ca-enriched edible mushrooms has been a growing research area. Through the incorporation of Ca into active biomacromolecules during the metabolic process, the mycelium and the fruiting bodies of edible mushrooms are able to convert inorganic-state Ca to organic-state Ca, which has higher bioavailability and is safer compared to the inorganic form [38][54]. Several studies have been conducted to investigate the capacity of edible mushrooms, including Pleurotus eryngii, Lentinula edodes, Hypsizygus marmoreus, Pholiota nameko and Ganoderma lucidum, to accumulate calcium from a variety of Ca sources [55][56][57][58][59][60]. Ca content (Table 1) in edible mushrooms highly depends on several factors, for example, edible mushroom species, growing environments, etc. [50]. Edible mushrooms, for instance, Flammulina velutipes [60], P. ostreatus, H. marmoreus, Auricularia auricula [61][62], Coprinus comatus, are excellent calcium-enriched candidates (Table 1). Generally, the total calcium is lower in edible mushrooms than in vegetables [63][64]. In an effort to enrich edible mushrooms with calcium, Tabata and Ogura found that the Ca level in fruiting bodies of H. marmoreus was improved as potato sucrose agar (PSA) and sawdust media were added with 1.0% Ca salts [65]. Choi et al. determined the calcium-enriching effect of P. eryngii in sawdust medium with a supplement of calcined starfish powder [66]. These authors also expected that numerous environmental factors, such as pHs, moisture concentrations, climate conditions, etc., could have an additional influence on calcium accumulation within the fruiting bodies of edible mushrooms [66]. In addition, the abilities of P. ostreatus and P. nameko to accumulate calcium in PSA and sawdust media have also been well characterized [59][67].
Table 1. Calcium level in some edible mushrooms.
Edible Mushrooms Levels (μg/g) References
Agrocybe aegerita 203.99 ± 6.47 Lin et al., 2015 [48]
Flammulina velutipes 890.34 ± 17.80
Hypsizygus marmoreus 1279.12 ± 25.58
Lentinus edodes 840.39 ± 5.23
Pleurotus eryngii 796.03 ± 15.92
Agaricus blazei murrill 425.81-703.79 Liu et al., 2018 [49]
Agrocybe cylindracea 115.21-564.40
Auricularia auricula 1971.83-6103.99
Coprinus comatus 1014.67-1874.72
Cyptotrama chrysopeplum 58.25-259.83
Dictyophora indusiata 86.35-475.48
Flammulina velutipes 32.62-164.09
Hericium erinaceus 13.49-25.23
Lentinus edodes 154.96-650.09
Pholiota nameko 282.76-740.47
Pleurotus eryngii 23.29-47.50
Pleurotus ostreatus 681.56-1143.17
Tremella fuciformis 88.03-691.07
Volvariella volvacea 925.59-1613.94
As one of the typical edible mushrooms, P. eryngii is acknowledged as an antioxidant resource, containing a large number of beneficial compounds and secondary metabolites, which may prevent oxidative damage [68]. It is also regarded as a high-efficiency calcium accumulator and can change inorganic calcium into organic calcium [69][70]. Akyuz et al. found that P. eryngii tended to have higher mineral accumulations, because the Mg and Ca contents in fruiting bodies were higher than other minerals [71]. Similarly, increased Ca content (14.94 mg/100 g) was observed in P. eryngii cultured on rice straw [72]. These differences in the calcium contents of P. eryngii were also attributed to the different culture media used or different substrate components. Moreover, the wide variation in the Ca content of P. eryngii grown on different media was similar to previous investigations [73][74][75]. In 2023, He et al. investigated the influence of five kinds of exogenous calcium sources (calcium chloride, calcium amino acid chelate, calcium lactate, calcium nitrate and calcium carbonate) on P. eryngii mycelia and fruiting bodies and found the optimum exogenous calcium (calcium lactate) could improve the yield of P. eryngii fruiting bodies and shorten its growth cycle [69]. However, in the investigation of Bu et al., the authors found different edible mushroom species (Pleurotus nebrodensis, P. eryngii and Pleurotus citrinopileatus) showed a significant effect on calcium enrichment. In addition, P. nebrodensis was a more suitable Ca-enriched edible mushroom candidate compared to other kinds of edible mushrooms [18].
In general, the main Ca metabolic products present in edible mushrooms are in an organic state. The distribution of Ca metabolites in edible mushrooms differs according to the cultivated cultivar and growing conditions. Specifically, 62.4% of Ca was combined with protein in Cordyceps sinensis, and the polysaccharide fraction contained 11.5% of Ca. A total of 80.5% of inorganic Ca was transferred into organic Ca [20][59]. The calcium enrichment of Laetiporus sulphureus showed similar findings. The degree of organic calcium reached 85.85% when the calcium content was 100 mg/L [54]. However, for Poria cocos, although 97.91% calcium was absorbed, only 24.57% organic calcium was detected [76][77].
Although edible mushrooms are excellent at accumulating Ca and can be grown over a wide range of Ca levels, their abilities to accumulate Ca differ from cultivar to cultivar and with culturing conditions, Ca sources and dosages (Table 2). Particularly, Ca sources and doses can highly affect Ca enrichment in edible mushrooms (Table 2). Current studies on Ca accumulation in edible mushrooms principally use CaCO3, CaCl2 and Ca(NO3)2 as Ca sources [78]. F. velutipes is one type of popular food in China due to its excellent anti-cancer and immunostimulating abilities [60][79][80]. Fan et al. showed that with the addition of 1~2% light CaCO3 and 1~2% shellac, the mycelia of F. velutipes grew denser, and the output and the quality of fruiting bodies improved [60][80]. In addition, in support of these results, it has been shown that adding 0.5% CaCO3 into potato sucrose agar (PSA) medium slightly enhanced the mycelium growth of H. marmoreus, while adding 5.0% CaCO3 into the same medium resulted in total inhibition [65]. However, it was observed that adding Ca phosphate and Ca carbonate into sawdust media did not affect the growth of P. eryngii cultivated on both potato dextrose agar (PDA) and sawdust media with a supplement of Ca salts, while adding CaSO4 inhibited the growth of mycelium [81].
Table 2. Calcium enrichment in some edible mushrooms.
Edible Mushrooms Calcium Source Optimized Ca Content for Enrichment (mg/L *) Calcium-Enriched Amount (mg/100 g **) References
Ganoderma lucidum CaCl2 200 100.6 Lee et al., 2006 [82]
Hypsizygus marmoreus CaCl2 100 2239.8 Zhang et al., 2022 [57]
Inonotus obliquus Ca(NO3)2 1000 21 Yu et al., 2016 [83]
Pleurotusnebrodensis CaCl2 6000 790.6 Bu et al., 2009 [18]
Pleurotusostreatus CaCl2 6000 491.67 He et al., 1998 [84]
Poria cocos CaCl2 2000 89.11 Wang et al., 2007 [76]
* mg/L of cultivation medium, ** mg/100 g of dry mycelium weight.
Different sources of calcium are commonly used in the commercial production of Agaricus spp. Thus, calcium sulfate (gypsum) is used as an ingredient in mushroom compost formulations and is applied in the early stages of the composting process, mainly for colloid flocculation, making the compost less greasy, improving aeration and subsequently facilitating mycelial growth [85][86][87][88][89]. Spent lime obtained in the production of sugar from sugar beet, consisting mainly of calcium carbonate, is used as ingredient of casings. The technical interest in the use of spent lime is basically due to its buffering capacity and its ability to improve the casing layer structure, giving casing soil a more or less dense texture [90][91][92]. Other sources of calcium have been evaluated in casings for the production of Agaricus subrufescens [93]. Calcium chloride can be used in irrigation water to improve the quality of fruit bodies, mainly their texture and dry matter content [94][95][96][97][98][99]. Irrigation with calcium lactate solutions has also been proposed [94]. The dipping of mushrooms in solutions of calcium chloride, calcium lactate and calcium nitrate has been evaluated in order to preserve the quality and increase the postharvest life of button mushrooms [100].
Inedible Ca sources have been used, such as agricultural lime, starfish powder, eggshells, oyster shells etc., which contain CaCO3 as the major component [101][102]. Accordingly, the bioconversion of inedible calcium sources is a good method for utilizing these renewables [64]. Zhang et al. found the mycelia of H. marmoreus grew more densely when 3.0% light CaCO3 or 3.0% shell powder was added into the medium [103]. In addition, for calcium enrichment in P. eryngii, Choi et al. found that supplementing sawdust medium with 1.0% oyster shell powder did not inhibit the mycelium growth of P. eryngii. The addition of 2.0% oyster shell powder into sawdust medium potentially elevated the calcium level within the fruiting bodies of P. eryngii up to 315.7 ± 15.7 mg/100 g, without prolonging the duration of spawning run, and delaying the days to primordial production. However, adding over 4.0% oyster shell powder into the sawdust medium resulted in the significant suppression of mycelial growth [101]. Furthermore, in Choi’s group, the authors found that the Ca level within the fruiting bodies of P. eryngii was improved through calcined starfish powder treatment. Supplementing the sawdust medium with 1.0% starfish powder did not inhibit the mycelial growth of P. eryngii and elevated the calcium level up to 256.0 ± 16.3 mg/100 g within the fruiting bodies of P. eryngii without prolonging the spawning period and delaying the occurrence of primordial germination [66]. These findings demonstrated that the development of calcium-fortified edible mushroom foods could be achieved using inedible calcium sources.
Typically, low Ca content stimulates the growth of edible mushrooms, while a high level of Ca suppresses the growth of mycelia and can even cause toxicity, with the feature of declined biomass and decomposed cells in edible mushrooms. The reason was that low Ca contents might activate enzymes in edible mushrooms, whereas high Ca contents might inhibit enzyme activity in the mycelia [104]. H. marmoreus, known as the Jade mushroom, exhibits many advantages to our health, including immunity-boosting, cancer-fighting and aging-preventing properties [57][103]. The mycelium growth of H. marmoreus was promoted at low Ca contents (500~2000 mg/L) but inhibited at higher contents (>2000 mg/L) [105]. Likewise, Sun et al. demonstrated that adding 60 mg/L CaCl2 into PDA medium promoted the mycelium growth of H. marmoreus. The effect of 50~100 mg/L calcium content on the mycelial growth rate was not significant, while at high concentrations, CaCl2 significantly inhibited the mycelial growth [106]. Interestingly, the optimal growth and calcium enrichment of G. lucidum was achieved when Ca(NO3)2 (600 mg/100 g) was added into the medium. The calcium enrichment of G. lucidum was significantly reduced when the addition level exceeded 800 mg/100 g [60][107]. Furthermore, Ca contents (0~2.0 g/L) did not inhibit the mycelium growth of Wolfiporia cocos. Calcium enrichment in the mycelia was as high as 89.11 mg/g [76]. A similar growth phenomenon has also been observed in P. ostreatus [108], L. edodes [102] and C. comatus [109].
Organic and inorganic Ca salts affect edible mushroom growth in different ways. In general, edible mushrooms are more responsive to organic Ca salts. Qin et al. investigated the influence of four kinds of calcium sources (CaCO3, CaCl2, Ca(NO3)2 and amino acid calcium) on the calcium accumulation ability of G. lucidum and found that the strongest ability to accumulate calcium was observed with 0.2% Ca(NO3)2 or when amino acid calcium was added. The amount of enriched calcium in G. lucidum reached 584.13 mg/100 g [60][110]. Similar results were observed for L. edodes. Chen et al. found that all calcium compounds (CaCO3, calcium lactate, CaSO4, CaCl2 and Ca(NO3)2) except calcium nitrate had a significant promoting effect on mycelial growth, and calcium sulfate was most advantageous to mycelial growth, whereas calcium lactate, as a result, was the most suitable as a calcium source to enrich calcium in mycelia [111]. Furthermore, the combination of calcium salts was also adopted to enrich calcium in C. sinensis. With the combination of calcium sources (40% Ca(NO3)2 + 60% CaCO3) at a total Ca2+ addition of 3.0 g/L, the biomass of C. sinensis could reach as high as 32.1 g/L [20].

This entry is adapted from the peer-reviewed paper 10.3390/jof9030338

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