Spent substrate from mushroom cultivation: exploitation potential toward various applications and value-added products (2024)

• Valorization of spent substrate is crucial for a sustainable mushroom industry.

• The review covers spent mushroom substrate (SMS) valorization for multiple uses.

• SMS composition and mushroom species are essential factors for its exploitation.

• SMS valorization forms an integral part of cascade use of plant biomass.

Table 1.

Reuse of spent mushroom substrate (SMS) for the cultivation of various mushroom species as reported in pertinent publications: origin and composition of SMS, mushroom to be cultivated, new substrate formulation and supplements, biological efficiency (BE) reported for the crop obtained and main comments on the results of the respective study. Abbreviation used: NR, not reported.

Table 2.

Reuse of spent mushroom substrate (SMS) as animal feed based on the outcome reported in pertinent publications. Abbreviations used: ADF, acid detergent fiber; ADL, acid detergent lignin; HWE, hot water extract; NDF, neutral detergent fiber; NR, not reported; S-SMS: steam-treated SMS; UN-SMS: untreated SMS.

3.1. Spent mushroom substrate in the diet of poultry

The incorporation of SMS derived from the cultivation of P. eryngii, P. ostreatus and H. marmoreus (fermented or not by Bacillus subtilis) at a ratio from 5 to 15% (w/w) in a poultry diet increased the feed intake without having adverse effects on the egg production and the mass of useful meat [^67,74,75,79]. On the other hand, incorporation of Agaricus blazei SMS at rates exceeding 0.4% (w/w) caused a gradual reduction in the weight gain of broiler chickens, while inclusion ratios of only 0.2% exhibited the highest value of weight gain and feed intake, as well as the best feed conversion [⁸¹]. Similarly, low inclusion ratios of P. sajor-caju SMS (up to 0.67%) improved the weight gain of broiler chicks in the first 21 days [⁸⁰].

3.2. Spent mushroom substrate in the diet of monogastric animals

SMS inclusion in the diet of monogastric animals have been tested with both pigs and model animals (mice, rats). The addition of sawdust-based SMS from Grifola frondosa (25% w/w) in rats’ diet did not affect the weight gain, the feed efficiency, or the biochemical parameters, while fecal weight and protein content were found to be higher [⁷⁶]. In addition, the – orally administered – hot water extract of SMS from Ganoderma lucidum exhibited enhanced murine immune function in mice [⁶⁵]. Furthermore, the use of low amounts of SMS from P. ostreatus (up to 3.5%, w/w), Cordyceps militaris (0.2%, w/w), and L. edodes (3%, w/w) in pigs’ diet positively affected the feed intake and conversion, as well as the final weight and quality of meat deriving from trials [^55,64,82]. C. militaris SMS resulted in increased immunoglobulin A and G, and glutathione peroxidase activities, while leukocytes, cholesterol and malondialdehyde contents were decreased [⁵⁵]. Similarly, beneficial effects on the intestinal mucosal barrier, immunity, and the diversity and abundance of the bacteria in the colon and cecum were observed for weaned piglets when fed with L. edodes SMS [⁶⁴]. It is noteworthy that SMC seems to be useful as a ‘behavior regulator’ in pigs; by having access to mushroom compost through a metal grid, pigs demonstrated significantly reduced negative behavior (e.g. such as nosing, tail biting and chewing) against penmates, as well as improved overall welfare in comparison to pigs with no access to SMC [⁸⁴].

3.3. Spent mushroom substrate in the diet of ruminants

The use of SMS as animal feed has been investigated to a larger extent for ruminants than for monogastric animals (i.e. 13 vs. 5 publications appeared, respectively, when a Scopus search was performed by using the keywords ‘Spent Mushroom substrate/compost’ AND ‘feed;’ July 2022). Incorporating SMS from various mushroom species at a rate of up to 30% (w/w) in the daily intake of ruminants revealed its potential as a supplement to conventional feeds without affecting several relevant parameters (Table 2). Specifically, feeding sheep for three weeks with a diet including up to 20% (w/w) of A. bisporus SMS did not affect the nutrient intake, digestibility, and nitrogen balance [⁸³]. Similarly, A. bisporus SMS fed at a rate of 15% (w/w) for 170 days did not cause any effect on the carcass and internal organs of Holsteins male calves [⁷³]. Plain P. ostreatus SMS in ratios higher than 15% resulted in adverse effects in sheep slaughter weight, empty body weight, and hot and cold carcass weight [⁶⁹]. In contrast, when rice straw was fermented for eight weeks with P. sajor-caju SMS before being fed to alpine dairy goats, it increased the rumen degradable fibers fraction and improved dry matter intake and milk yield [⁶¹].

Feeding male sika deer for 60 days with P. ostreatus SMS (10%, w/w) resulted in a reduction of the intake of organic matter and improved digestibility of crude fibers, while no effect on either the apparent nutrient digestibility, feed intake, velvet antler production, or biochemical indexes was observed when F. velutipes SMS (10%, w/w) was fed to the same animals [⁶²]. When hot water extracts from G. lucidum and Ganoderma chalceum (syn. G. balabacense) SMS were supplemented to dairy cow feed, immunity and antioxidant capacity were increased, and milk quality was improved [^71,72]. By using SMS extracts, the addition of large amounts of fibrous components from the untreated SMS could be avoided, but further studies are required to investigate their impact on animal health and the optimum incorporation rate, which depends mainly on the substrate origin.

Agaricus and Pleurotus species are usually cultivated in straw-based substrates, while L. edodes, G. lucidum, Gr. frondosa and He. erinaceus are cultivated in wood-based substrates. The incorporation rate of such substrates in animal feed is low, and further treatment is necessary to improve their nutritional characteristics. In recent years, microbial fermentation with probiotic microorganisms has been adopted as a cheap, fast, and efficient method to reduce fibrous ingredients and upgrade the protein content of SMS, including those deriving from sawdust-based media. Moreover, probiotic microorganisms relieve animals weaning stress, regulate intestinal microbiota, and reduce diarrhea incidents [^85,86].

Due to its high moisture content, SMS tends to decompose rapidly; hence, it needs to be processed quickly. This could be achieved by ensiling, for instance, by lactic acid fermentation under anaerobic conditions [⁸⁷]. Lactic acid bacteria produce desirable metabolites, and suppress the growth of clostridia and other deleterious microbial populations [⁸⁸]. Although ensiling processes may be initiated naturally by the epiphytic microorganisms existing in the initial material, they can be assisted by inoculated bacteria. Inoculation of SMS with Lactobacillus, Bacillus, or Enterobacter spp. ensures rapid acidification, and increases dry matter degradability and crude protein content [^{64,66,70,75,77,78}].

An indicative example is the use of a sawdust-based P. eryngii SMS incorporated at a high rate (45%, w/w) into silage with various agricultural by-products, and fermented for 22 days [⁶⁸]. Using the resulting product for feeding sheep resulted in similar energy value, lower digestion of fibers, and higher protein metabolism and utilization compared to the outcome achieved with a rye straw-based control diet. In addition, the sawdust-based SMS from the same mushroom species, when fermented with Enterobacter and Bacillus spp., significantly improved growth performance and carcass traits in Hanwoo steers compared to rice straw feed administered for 12.6 months during the growing and fattening periods [⁷⁷]. Similarly, P. ostreatus SMS fermented with Lactobacillus plantarum and Pediococcus acidilactici could replace up to 50% of the conventional feed provided to Hanwoo steers and postweaning calves [^66,70,78]. Such an SMS-based feed improved the growth performance of the tested animals or enhanced the daily gain caused by increased voluntary feed intake. Finally, feeding Liuyang black goats with P. ostreatus SMS co-fermented with whole rice plants improved meat quality and had no adverse effects on the slaughter performance [⁶³].

3.4. Spent mushroom substrate in the diet of fish and edible insects

Using SMS in pisciculture is also of substantial interest. SMS from P. ostreatus, Pleurotus cystidiosus, and G. lucidum seems to support the growth of catfish, and significantly increase its survival rate and digesting ability compared to commercial feeds [⁸⁹]. The addition of C. militaris SMS up to 40 g kg⁻¹ in the diet of Nile tilapia (Oreochromis niloticus) improved growth performance, skin mucus lysozyme, and peroxidase activities, as well as serum immune parameters [⁹⁰]. The combination of SMS with L. plantarum further improved those parameters. Moreover, enrichment of Nile tilapia diet with A. blazei SMC (1%, w/w) provided significant protection against infections from Streptococcus agalactiae [⁹¹]. Including an extract from the SMS of Schizophyllum commune, a popular mushroom in Thailand, in the feed of Nile tilapia resulted at enhancing their immune defense [⁹²].

In the frame of the need to reduce dependence on feeds deriving from plants, the use of insects seems to be a promising alternative due to their high content in crude protein (up to 76%) and fat (up to 59%), energy (20–30 MJ/kg DM), as well as to their short life-cycle and the low-cost growth prerequisites [^93–95]. The potential of six SMS derived from Auricularia cornea, Auricularia heimuer, P. eryngii, P. ostreatus, Pleurotus citrinopileatus, and L. edodes was recently evaluated to rear black soldier fly (Hermetia illucens) and Tenebrio molitor larvae. L. edodes SMS was shown to be the most suitable to replace the insects' conventional feed [^96,97]. Furthermore, when Protaetia brevitarsis larvae were grown on L. edodes or Auricularia auricula-judae SMS, a nutrient-rich organic fertilizer with low phytotoxicity and high humic acid content was produced [⁹⁸]. However, no studies exist on the production of insects naturally feeding on mushroom substrates. That could be a promising alternative considering the ease of insects’ growth and the low demand in terms of material resources.

In conclusion, using SMS in animal nutrition can significantly contribute to the enrichment of feed, particularly regarding proteins and bioactive compounds. However, incorporating SMS into the daily feed-schedule is a complex process. The mushroom species, the initial substrate composition, the animal species, and the digestibility and voluntary intake of the final product are factors that must be carefully considered to calculate the final integration rate. The high NDF and ADF content (especially in sawdust-based substrates) is probably the main limiting factor in SMS exploitation as feed. Adopting appropriate treatment approaches, including lactic acid fermentation and the use of SMS extracts, could enhance the nutritional and acceptance characteristics, thus facilitating the incorporation of SMS in the diet of productive animals. Particularities related to the composition of each type of SMS and the individual needs of the animal species require careful experimentation on a case-by-case basis to ascertain the safe and efficient use of SMS.

4.1. Use of spent mushroom substrate as biofertilizer and soil conditioner

Organic soil amendments, commonly used in agriculture, exert positive effects on crop productivity and soil health by affecting physicochemical and biological properties of soil [^101–103]. Among the most widespread materials used as organic soil amendments are those originating from municipal wastes (food and gardening wastes, sewage sludge), animal husbandry (manure), crop production (stems, leaves and branches), and agro-industrial activities (fruit pulp and oil extraction by-products). However, those materials can contain hazardous compounds or plant pathogens, which are detrimental to soils and crops.

Since SMS is rich in nutrients and has low (and, most often, no) content in xenobiotic compounds and heavy metals, it can be used as a soil amendment either directly or after a composting treatment. SMS properties vary depending on the raw materials included in the initial substrate, the mushroom species, and the cultivation technology. Accordingly, a wide range of effects is noted on soil characteristics, crop growth and yield when SMS is used as a soil conditioner or fertilizer [^104,105]. However, it is worth mentioning that the mushroom species and the SMS composition are often not specified in pertinent publications, making it difficult to draw sound conclusions about its exploitation prospects.

A summary of relevant reports on incorporating SMS into soils is presented in Table 3, which includes information on the SMS origin, type, and incorporation rate, and the main effects of SMS addition on the soil and plants under study. The presented results indicated improvements in soil structure and fertility, which led to increased crop production or contributed to the restoration of barren lands and degraded soils.

By applying SMS of unknown origin (20 Mg ha⁻¹) and chicken manure (10 Mg ha⁻¹) in a sandy soil every one-two years for 20 years, Lipiec et al. [¹⁰⁹] reported an increase in soil organic matter content by 102–201%. The experiment also resulted in a long-term increase in field water capacity caused by the augmentation of residual pores by up to 251%. Similarly, fresh or composted SMS applied annually for four years at two different rates (8 and 25 Mg ha⁻¹) to a semiarid vineyard soil increased the content of inorganic N in the soil surface (0–5 cm) [¹²⁰]. However, only the highest SMS addition rate improved soil organic carbon, total nitrogen, and labile organic forms at 0–5 and 5–15 cm soil depths.

In other large-scale applications, incorporating A. bisporus SMS into the soil (100 kg ha⁻¹) increased oxidizable organic carbon, organic N, and available P content [¹¹⁹]. The values obtained for using A. bisporus SMS alone were higher than those resulting from incorporating a mixture of A. bisporus and P. ostreatus SMS (1:1, v/v). Both schemes of SMS addition resulted in increased phosphatase activity compared to unamended soil, while no alterations in the soil salinity or pH value were observed, and N mineralization was low. The same treatments also had positive effects when examined in a calcareous clayey-loam soil used for lettuce production [¹⁰⁵]. In that study, application of SMS resulted in higher values of oxidizable organic carbon, organic N, extractable K, available P, and cation exchange capacity (especially when using A. bisporus SMS) than in soils receiving NPK fertilization, while lettuce yields were similar.

Ngan and Riddech (2021) reported the application of a mixture of SMS with plant growth-promoting bacteria (Bacillus amyloliquefaciens) in the cultivation of Hibiscus sabdariffa [¹¹⁰]. The study revealed an improvement in soil properties exceeding the effect exerted by NPK fertilization. Unfortunately, the lack of information on the SMS origin makes it difficult to compare the results with those of other relevant studies.

Testing fresh or sterilized F. velutipes SMS in cucumber cultivation resulted in a significant increase in total organic carbon, dissolved organic carbon, and microbial biomass carbon compared to NPK use and to no fertilization [¹¹¹]. The study revealed higher levels of microbial diversity and enzyme activities for the fresh SMS-amended soil compared to soil treated with mineral fertilizer. Correspondingly, A. bisporus SMS amendment in soils increased bacteria and fungi co-occurrence, and the plant yield was positively affected by the relative abundance of microbial hubs [¹¹²]. Similarly, the application of Agaricus subrufescens and L. edodes SMS enhanced soil microbial population, and resulted in a remarkable increase in lettuce plants' dry weight compared with the results achieved with no fertilization or NPK treatments [¹⁰⁴]. For several other crops, SMS application to the soil led to higher yields than those obtained by mineral fertilization [^105,116,121].

Soil biological properties play a critical role in the maintenance of ecosystem functions, crops productivity enhancement, and at mitigating the adverse effects of pollutants. The beneficial effect on soil biological properties, including the structure of microbial communities and associated enzyme activities, is an attractive aspect of using SMS as an amendment. The main disadvantage of SMS is the state of stability/maturity which – if imperfect/immature – could hamper its wide agronomic use. However, this issue could be overcome by composting it, alone or mixed with other crop residues, under controlled conditions [¹¹⁵].

Several studies have revealed that using SMS as an ingredient in the composting process promotes the degradation of organic matter in mixtures with waste sludge, pig manure, corn stalks, and cow dung [^122–124]. It has also resulted in the enhancement of the humification process [¹²⁵], at reducing ammonia emissions [^122,126], facilitating heavy metal passivation [¹²⁵], and improving the quality of the final product [^122,124]. Furthermore, using composted A. bisporus SMS alone as a substrate for the cultivation of Lolium multiflorum resulted in a yield improvement by up to 300% compared to the reference of NPK fertilization [¹¹⁵]. Co-composting of Au. auricula-judae SMS with biogas residues and pig manure led to the production of higher quality seedlings than those obtained from commercial substrates [¹¹³]. Substrates containing composted A. bisporus and P. ostreatus SMS resulted in increased yields of baby leaf lettuce, even in the presence of the soil-borne plant pathogen Pythium irregulare [¹⁰⁸]. Adopting appropriate methodologies, such as the addition of enzymes or earthworms (vermicomposting), during the composting process should result in further improvement of the quality of composted SMS by promoting the beneficial effects of autochthonous bacteria, increasing ion-exchange capacity, decreasing total carbon and C/N ratio, and promoting the synthesis of nitrates [^127–129].

In conclusion, the use of SMS as soil amendment has beneficial effects on soil fertility and structure. SMS presents a promising potential for substituting, at least partially, the use of mineral fertilizers in continuous crops and thus contributes at mitigating soil secondary salinization and acidification, and at avoiding nutrient imbalances and accumulation of toxic allelochemicals.

4.2. Use of spent mushroom substrate for plant-disease control

To deal with the negative repercussions of using chemical-based pesticides in agriculture, the application of environmentally friendly products for pest protection is crucial. Biocontrol agents, including live organisms and biological pesticides, are potential alternatives for controlling plant diseases. In contrast to chemical pesticides, biocontrol agents have little impact on non-targeted organisms; they do not leave behind any long-lasting harmful leachates and do not lead to the development of resistant microbial strains or insects. However, they often exhibit low-medium effectiveness and a shorter shelf life [^130,131].

The bioactive compounds in SMS have antimicrobial properties [¹³²], which could be exploited against plant pathogens. Although in vitro studies have shown the potential suitability of mushroom and mycelium extracts against plant pathogens [^87,133,134], they do not necessarily reveal the in vivo effectiveness. SMS application has shown to be effective in suppressing plant disease incidence. Table 4 shows examples of reported research findings on using SMS for controlling plant pathogens and pests, and also includes the SMS origin, the plant – pathogen/pest system, and the main outcome of each study.

Several studies on SMS-based biocontrol products against plant diseases concern L. edodes. The in vitro antimicrobial activity of L. edodes SMS [^87,151], was further evidenced when hot water extracts were used to inhibit the germination of Pyricularia oryzae conidia in rice plants and to suppress the growth of Phytophthora capsici in pepper plants [^141,142]. A chitin/cellulose nanofiber complex isolated from L. edodes SMS exhibited significant activity against Alternaria brassicicola in Arabidopsis thaliana plants [¹³⁵]. L. edodes SMS-based biocontrol agents reduced the disease symptoms and promoted plant growth [^135,142].

P. ostreatus SMS can provide another alternative to suppress plant diseases. Paddy straw-based P. ostreatus SMS, bio-fortified with Trichoderma asperellum, led to a remarkable reduction of the severity index of Fusarium oxysporum-induced disease, while it contributed to enhanced tomato growth [¹³⁷]. The application of a polysaccharide extract from P. ostreatus SMS and discarded L. edodes mushrooms reduced by 50% the severity of bacterial spot caused by Xanthom*onas gardneri in tomato cotyledons, leaflets, and five-leaf plants [¹³⁹]. Phenolic-rich extracts from P. ostreatus SMS have been shown to prevent the development of the parasitic plant broomrape in faba bean cultivars [¹⁵²], and to improve the rice growth and yield parameters [¹⁵³]. In another study, mixing composted SMS from either P. ostreatus or V. volvacea with a biofertilizer exhibited higher control efficacy against Ralstonia wilt and Phytophthora blight diseases, than using the biofertilizer alone [¹³⁸].

SMS from less widely cultivated mushrooms has also shown suppressive activity against plant diseases. Application of SMS from Ly. decastes and P. eryngii into soils used for cultivating cucumber resulted in protection against disease symptoms caused by Colletotrichum orbiculare, Podosphaera xanthii, Cladosporium cucumerinum and Pseudomonas syringae [^147,149]. A protective effect against Colletotrichum lagenarium in cucumber plants was observed after spraying a water extract of Ly. decastes SMS [¹⁴⁹]. The incorporation of Ly. decastes SMS into soil suppressed the lesions caused by Al. brassicicola in Arabidopsis thaliana leaves; this effect was attributed to SMS volatile components [¹³⁶].

The results so far indicate that SMS richness in antimicrobial compounds in concomitance with its natural microbiome, including organisms suppressing soil-borne plant pathogens, are essential prerequisites for developing relevant plant-disease control products. However, further experimentation, including evaluation in large-scale greenhouse and field trials, is required to fully benefit from that potential toward a solid sustainable agriculture model.

4.3. Effects of SMS on nutritional value and secondary metabolites production in plants

Plant secondary metabolites, including vitamins, terpenoids and polyphenols, in fruits and vegetables are important for reducing risks of cardiovascular diseases and maintaining good health [^154,155]. Those molecules exert a wide range of effects on the plant and associated organisms, and their production depends on various biotic and abiotic factors [¹⁵⁶].

SMS application affects the content of secondary metabolites in plants. Vahid Afa*gh et al. [¹⁵⁷] reported that the incorporation of Agaricus SMS leachates in sandy soil (up to 15% (v/v)) significantly increased the content of essential oil, proline, and soluble sugars in chamomile (Matricaria chamomilla) in comparison to plants grown on non-supplemented soil. Increasing the SMS leachate content enhanced K and Na absorption, whereas N and P uptake was not affected. Similarly, the addition of SMS leachate (20–60% (v/v)) in the soil led to increased content of essential oil components, chlorophyll, and antioxidant compounds in chamomile [¹⁵⁸]. Application of SMS as an amendment in soils where basil (Ocimum basilicum) was cultivated, resulted in a two-fold increase in essential oil components, and in an enhancement of its content in micro- and macronutrients [¹⁵⁹].

SMS use in the cultivation of vegetables demonstrated a wide range of effects on the various parameters, including product yield and quality. Applying a leachate of P. ostreatus SMS and A. bisporus SMS (10–25% (w/w)) to the soil increased the content of chlorophyll in pepper leaves, and that of carotenoids and protein in fruits [¹⁶⁰]. Furthermore, A. bisporus SMS biofortified with Trichoderma harzianum inhibited lipid peroxidation and protein oxidation with a significant increase in total polyphenol and flavonoid contents in tomatoes, and enhanced Fe^2+/Fe³⁺ chelating activity and superoxide anion radical scavenging activity compared to an SMS-free control [¹⁶¹]. Similarly, P. ostreatus SMS biofortified with Trichoderma asperellum improved morpho-biochemical and nutritional parameters, such as the content of chlorophyll, carotenoids, total soluble sugars, total soluble proteins, lycopene, β-carotene, and ascorbic acid, and antioxidant properties, of tomato plants [¹³⁷]. Another study, using SMS from A. bisporus or P. ostreatus for replacing peat moss by 25–100% (w/w), reported that the effect of SMS on the macronutrient content of tomato, courgette, and pepper plants was species-dependent [¹⁶²]. A proportional increase of N content with the increase of SMS ratio in the substrate was observed for pepper, whereas no significant effect was evident for courgette and tomato. In addition, increasing the incorporation volumes of SMS increased K content for courgette and pepper, but not for tomato. Last, courgette and pepper exhibited similar P content when grown on SMS-based substrates and a peat control, whereas P content in tomato seedlings grown on SMS-based substrates was lower than in plants grown on peat.

Although the scientific data on the effects of SMS on the nutritional value of edible and medicinal plants are still limited, the available results reveal SMS potential to increase the content of specific elements and secondary metabolites in plants.

5.1. Enzymes

SMS is a source of various enzymes that can be recovered by extraction with different solvent systems. Furthermore, SMS can be used as substrate for the cultivation of enzyme-producing microorganisms.

5.2. Bioactive compounds

SMS contains bioactive compounds of different functionality and origin. The fungal mycelium contains polysaccharides, sterols, proteins, polyphenols, vitamins, and other bioactive molecules. Mycelial growth throughout the surrounding environment also results in the secretion of potentially useful bioactive compounds. In addition, the extractive fraction of the lignocellulosic substrate and the oligomeric products from fungal degradation of polysaccharides and lignin might also be sources of bioactive substances. However, while the bioactive molecules of the sporocarps of edible fungi have been extensively investigated [¹⁹²], the information on the bioactive potential available in SMS is still limited. Recovery of bioactive compounds is a promising direction for valorizing SMS.

6.1. Case study 1: food – ethanol – solid fuel

The integrated production of L. edodes mushroom (food) and biofuels from hardwood residues can be an example of cascade use [^{16,187,206,207}]. Food (mushrooms) is produced on a lignocellulosic substrate. Concomitantly, mushroom cultivation selectively degrades lignin and hemicelluloses, thus facilitating the enzymatic saccharification of cellulose. Glucose from the saccharification process can then be fermented to ethanol using yeast. Enzymatic saccharification also generates lignin-rich solid leftovers, which can be used as a solid fuel (Figure 4).

From a circular bioeconomy point of view, the forest residues can be considered primary bioresources from forest production (c.f. Figure 3). Exploiting the forest residues as mushroom growing substrates results in the production of fruitbodies as primary products. SMS is the secondary bioresource and can be converted to the secondary product ethanol. Ethanol can be used to synthesize renewable polyethylene to produce green plastics or for fuel applications, including advanced jet biofuels. After cellulose saccharification, the solid leftover can also be recovered as a tertiary bioresource/biowaste, and converted to solid fuel, a ‘tertiary product.’ A recently published mass balance analysis revealed that one ton of birch-based initial mushroom substrate might result in about 600 kg of fresh shiitake (L. edodes) fruitbodies (90% moisture), 130 liter of ethanol, and 300 kg (dry mass) of solid biofuel [¹⁸⁷]. This system/approach can also be applied to other mushroom species. Using an experimental setting like the one used for L. edodes, Chen et al. [²⁰⁹] found that one ton of birch-based initial substrate might result in about 400 kg of fresh fruitbodies (90% moisture) of Au. auricula-judae, 35 liters of ethanol, and 300 kg dry mass of solid biofuel. The solid fuel was found to have a relatively high calorific value and favorable characteristics for direct combustion to produce heat. The generated heat can be used for the pasteurization of substrates or space heating.

The outcome of the production chain can be affected by the composition of the initial substrates used for mushroom cultivation. Chen et al. [²⁰⁶] reported that alder-based substrate led to 4% more mushroom fruitbodies, 14% more ethanol, and 23% more solid fuel than birch-based substrate. On the other hand, an aspen-based substrate resulted in a 37% lower yield of fruitbodies than the birch-based one, although the yields of ethanol and solid fuel were comparable for substrates from both tree species.

The same concept is also applicable to other biofuels. For instance, another ‘food – biofuel – solid fuel’ alternative is to produce biogas instead of ethanol as a secondary product. Lin et al. [²¹⁰] cultivated shiitake on woodchips and produced biogas by anaerobic digestion (AD) of SMS; at the end, around 53–57% (dry mass) of the substrate was solid leftover. Since the AD process consumes mostly carbohydrates [^211,212], the leftovers are expected to have a relatively high content of lignin, a component with a high calorific value. Therefore, using the leftovers as a solid fuel for a self-supporting heating system could be meaningful. In a slightly different alternative, rice straw was used as the main ingredient for P. ostreatus substrate, fruitbodies were produced as the primary product, SMS was directed to AD for producing biomethane as a secondary product, and the AD digestate was used as biofertilizer (tertiary product) for rice cultivation [²¹³].

6.2. Case study 2: food – biogas − 2^nd cycle mushroom

Another example of a cascade system was reported by Ikeda et al. [²¹⁴] using the mushroom ‘enokitake’ (F. velutipes) cultivated in a substrate based on corncobs supplemented with rice bran. In this case, agricultural residues were the primary bioresource, and enokitake fruitbodies were the primary product. The SMS resulting after mushroom harvest was anaerobically digested for producing biogas, the secondary product. After the AD process, around 45% of the initial mass was left as solid residue or digestate. In the next step, KOH or NaOH was used for pretreating the AD residue (SMS-ADR), which was then mixed with rice bran at a 50:50 weight ratio for formulating a new substrate to be subsequently used for a second enokitake cultivation cycle. The results were promising: the yield of the tertiary product, i.e. mushrooms cultivated on SMS-ADR, was comparable to those of the primary one, i.e. mushrooms cultivated on corncob-based ‘standard’ substrate. Crude protein, ether-extracted compounds, crude fiber, minerals (Na, P, Ca, K, Mg), and free amino acids in fruitbodies showed similar content to those obtained from the standard substrates. The study did not discuss further use of the second cycle SMS (SMS-II). In our opinion, this cascading system could still be extended to a quaternary product by exploiting the potential of SMS-II as a biofertilizer or a soil amendment.

Cascade systems including biogas as the secondary product are also feasible for other mushroom species. Since lignin content decreases during the mushroom cultivation, the resulting SMS is accessible to anaerobic microbes, thus facilitating AD conversion of carbohydrates to biogas. On the other hand, after biogas production, and although data on the chemical composition of the digestate are not available [²¹⁵], the lignin content is expected to increase due to its recalcitrance to degradation by anaerobic bacteria [^211,212,216]. Therefore, it was wise to choose white-rot fungi again to break the recalcitrance of lignin to produce additional value-added tertiary products. Although the low pH and the presence of unknown by-products may inhibit a second mushroom cultivation cycle, it was shown that KOH or NaOH soaking was a viable method to improve the susceptibility of digestate to be further used for enokitake cultivation [²¹⁴]. Nevertheless, the precise mechanism behind the alkaline reactivation of the digestate from AD for mushroom cultivation remains to be clarified.

6.3. Case study 3: food − 2^nd cycle mushroom – enzymes

Another possible cascading chain can include two cycles of mushroom cultivation in a row followed by recovery of extracellular enzymes as a tertiary product. Economou et al. [¹⁹¹] reported a case study, where oyster mushroom (P. ostreatus) was produced on a wheat straw-based substrate, and the resulting SMS (SMS-I) was tested as the main ingredient of the substrate for a second mushroom cultivation cycle. After harvesting the fruitbodies from the second production cycle, the generated SMS (SMS-II) was used as a source for the recovery of the lignin-degrading enzyme laccase. Among the five fungal species tested for the second mushroom production cycle, P. pulmonarius resulted in the SMS providing the highest yield of laccase, 2465 U g⁻¹ day⁻¹ (dry mass based). The crude laccase extract was then used for the dephenolization of wastewaters [²⁶]. The authors did not explore possible uses of the solid stream remaining after laccase extraction from SMS-II. A potential extension of the cascading system would be possible by using that stream as either biofertilizer or solid fuel.

Using P. ostreatus as the species involved in the first step of the cascading system is a reasonable strategy considering that Pleurotus spp. are among the most studied white-rot fungi for biological treatments of lignocellulosic materials [²¹⁷]. Compared with other edible fungi, they have the advantages of presenting a relatively shorter life cycle, and broader adaptation to substrate assortments and growing environments. Even though Pleurotus lignocellulolytic enzyme activities are generally comparable to those of L. edodes [²¹⁵], the lignocellulose degradation capacity of the former is generally lower than that of shiitake, probably because of the shorter life cycle [²¹⁷]. It must be emphasized that the determination of SMS composition, which is essential for fully understanding the potential of the SMS to be directed to new cultivation cycles, is often underestimated in the literature.

The cultivation of white-rot edible fungi on primary bioresources results to food (mushrooms), and functions as a biological pretreatment for facilitating biochemical conversions. Therefore, mushroom cultivation is crucial in cascading systems of lignocellulosic biomass utilization. In addition to the case studies discussed above, many other cascade systems producing fruitbodies as a primary product, and including other products or services, can be proposed to valorize SMS and other residual streams. The feasibility of producing antibiotics [²¹⁸], antitumor sterols [⁵⁸], seedbed of vegetables [²¹⁹], fertilizers [¹⁰⁴], soil bioremediation agents [²²⁰], enzymes [¹⁷⁵], biochar [²²¹], and other products has been demonstrated. Some products could be considered as different ‘puzzle pieces’ to be chosen and integrated into a chain of cascade uses. However, appropriate approaches ensuring optimal process integration remain to be developed. Process integration has to be developed through interdisciplinary approaches to maximize system values for the circular bioeconomy and the protection of the environment. Furthermore, systematic evaluation (e.g. life cycle assessment) and optimization of processes for the cascading uses must be addressed.

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