Using of Appropriated Strains in the Practice of Compost Supplementation for Agaricus subrufescens Production

Introduction

An emerging Agaricus species, Agaricus subrufescens Peck, also named Agaricus blazei Murrill sensu Heinemann, Agaricus rufotegulis Nauta, or Agaricus brasiliensis Wasser, M. Didukh, Amazonas & Stamets, has been an actively cultivated mushroom in Brazil since 90's; when it was cultivated for first time in the Sao Paulo State and then extended to other regions close to the Atlantic coast (Farnet et al., 2014).

This ascend is because of the important medicinal proprieties of the mushrooms used for the treatment of cancer, leukemia, and hypertension, which are attributed to its active compounds, such as glycoproteins, β-d-glucans, saponins, steroids, tannins, polysaccharides, ergosterol, and fatty acids (Wang H. et al., 2013; Venkateshgobi et al., 2018). Previous studies reported that aqueous extracts of A. blazei offered the neuroprotective effect against the experimental model of Parkinson's disease and aging due to its anti-oxidant, anti-inflammatory, and anti-apoptotic functions (Nakanishi et al., 2014; Venkatesh Gobi et al., 2017, 2018).

During the last 5 years, various studies occurred involving several steps of production, with the objective of making commercial production more and more feasible, transforming family scale units to industrial scale production (Dias et al., 2013; Llarena-Hernández et al., 2014; Pardo-Giménez et al., 2014; Zied et al., 2014a; Carvalho Sousa et al., 2016).

Among the different steps of production, compost (formulation, phase I and II) is thought to be one of the most important, because it directly influences the productivity and quality of the mushrooms (Horm and Ohga, 2008; Matute et al., 2010; Llarena-Hernández et al., 2013; Wang J. T. et al., 2013; Souza et al., 2014). To improve the compost process, substrate supplementation has been used to provide nutrients to the developing mushroom, reducing the cultivation cycle and increasing productivity by up to 30% (Pardo-Giménez et al., 2012, 2016).

The practice of supplementation can be carried out at spawning, which does not demand additional production costs, except purchasing supplements that will be added to substrate. Currently, several companies commercialize supplements to be applied in the cultivation of Agaricus bisporus and Pleurotus ostreatus, although commercial supplement was not found for industrial scale of A. subrufescens production.

Therefore, the aim of this study was to analyse the efficiency of supplementation in A. subrufescens compost at spawning, with different sources of organic materials, using three commercial strains. In addition, this study considered the influence of the chemical characteristics of the supplements on the physiological development of the mushrooms.

Materials and Methods

Strains

Three commercial strains were used, including ABL 16/01 and ABL 16/02 (provided by the company Funghi & Flora, Valinhos, Brazil) used by growers in Sao Paulo State and ABL 16/03 (codified as CS7—Carvalho Sousa et al., 2016) used by growers in Minas Gerais State. The strains are deposited in the public culture collection of Sao Paulo State University, Câmpus de Dracena (FCAT/UNESP), which allows access to interested researchers. Spawns of each strain were produced on sterile sorghum-based substrate (Sorghum bicolor) supplemented with gypsum (160 g kg⁻¹) and lime (20 g kg⁻¹). All preparation and sterilization procedures were done in accordance with Zied et al. (2010, 2014b).

Compost

The compost was prepared using the traditional method, lasting 22 days of phase I and 10 days of phase II, totalling 32 days. The formulation used had a dry weight of 1,000 kg of Panicum maximum, 1,500 kg of sugarcane bagasse, 50 kg of soybean, 5 kg of urea, 5 kg of ammonium sulfate, 10 kg of superphosphate, and 40 kg of limestone. The bulk materials (P. maximum straw and sugar cane bagasse) were moistened for 9 days and rotated after 2 days. The concentrated materials (soybean, urea, ammonium sulfate, simple superphosphate, and lime) were added after each turning operation throughout the composting phase I (Table 1). The compost remained for 18 h at 59 ± 1°C for pasteurization and 8 days at 47 ± 2°C for conditioning during phase II of composting. The chemical characteristics of the compost at the end of phase II are listed in Table 1.

TABLE 1

Table 1. Operations performed during the composting process (phase I) and chemical analysis of compost at the end of phase II.

Supplement

Six supplements were used in the research and can be separated into four categories: (i) commercial supplements (Spawn Mate II SE^®–recommended to the production of P. ostreatus and Pro Mycel Gold^®–recommended to the production of A. bisporus, both of Amycel and Spawn Mate company, Watsonville, US); (ii) supplements based on agro-industrial wastes (20% grain or nut and 80% hulls provided of peanut waste and acerola waste—special seeds, obtained after the extraction of the juice); (iii) supplement-based noble grains (bran of soybean, corn, and cotton—a mixture of 33.3% each); and (iv) a mix of supplements (ii) and (iii) (peanut waste, acerola juice waste, and noble grains—a mixture of 33.3% each), which was used in order to provide a balance of the chemical characteristics of the three supplements presented in category (ii) and (iii). Supplements (ii), (iii), and (iv) were dried at 68°C for 24 h (which served as a heat treatment) until reaching 4–6% moisture and then were crushed with a < 0.5 mm sieve. Additionally, a substrate without supplement was used as a control. The chemical characteristics of each supplement used are listed in Table 2. The macro and micro nutrient content, organic matter (OM), C/N ratio, and pH were evaluated following the methodology presented by Bell and Ward (1984) and Sonneveld and van Elderen (1994).

TABLE 2

Table 2. Chemical characteristics of the supplements.

Supplementation at Spawning

At spawning or at the end of the Phase II composting process, supplements were added to the compost in the amount of 1% wet weight of compost. At the same time, the strains were added to the compost in the amount of 1.5% of spawn wet weight of compost. Therefore, in each bag, we deposited 4 kg of compost with 40 g of supplement and 60 g of spawn. Spawn run occurred under controlled temperature (26°C), relative humidity (80%) and carbon dioxide content (3,000 ppm) conditions and was delayed 18 days.

Casing Layer

Soil with 350 g kg⁻¹ of clay, 100 g kg⁻¹ of silt, and 550 g kg⁻¹ of sand was collected 2.0 m below surface, as recommended by Zied et al. (2011a), to produce A. subrufescens casing layer. Calcitic lime was added to the soil for pH correction as well as small fragments of charcoal in the proportion of 4:1 (v/v) to increase the porosity and reduce the density and compaction of the casing layer. When the mycelia were fully developed, the compost was pressed, and leveled to facilitate the addition of the casing layer to a height of 5 cm.

Production

The total production phase after casing addition was 90 days, with four flushes of mushroom harvested. The first one lasted 12 days, the second lasted 6 days, the third lasted 4 days, and finally, the fourth lasted 3 days. During the production, the air temperature ranged from 18 to 30°C, the compost temperature ranged from 20 to 28°C, and the relative humidity was between 85 and 90%. For primordial induction, the temperature was reduced to 2°C per day until reaching 20°C following the methodology presented by Zied and Minhoni (2009). The basidiocarps were harvested manually, followed by scraping the base of the stipe to remove the casing layer residues. The analysis was subsequently performed to quantify (i) the yield calculated as 100 times the wet weight of the mushrooms divided by the wet weight of compost, expressed as a percentage (1st, 2nd, 3rd, and 4th flush and total yield); (ii) the number of mushrooms harvested; and (iii) the weight per mushroom, expressed in grams (total fresh weight harvested during the cycle) divided by the number of mushrooms by bag, as previously described by Zied et al. (2014b), Pardo-Giménez et al. (2016), and Zied et al. (2017).

Statistical Analyses

The experiment was carried out using a double factorial, completely randomized design, with seven supplementations (six supplements + control) × three strains, totalling 21 treatments, each with six replicates (represented by a box containing 4 kg of wet compost). The variations between the chemical compositions of the supplements were analyzed considering the similarity by using the Nearest Neighbor Method. The means of each variable were compared by the least significant difference (LSD) test at p < 0.05 using SAS JMP software. Sigma Stat 3.5 software was used to calculate the linear correlations among the values for the yield (1st, 2nd, 3rd, 4th, and total), number, and weight of the basidiocarps and the chemical characteristics of the supplements.

Results

The supplements formulated in this study had the highest Ca-values. Commercial supplements (Spawn Mate and Pro Mycel Gold) and noble grains showed the highest values of N, P, K, Mg, S, and Zn and, in this sense, are characterized as supplements with high nutritional content (Table 2). According to Figure 1, the macronutrient and micronutrient contents, OM, C/N ratio, and pH-values of the commercial supplements were considered similar, by using the Nearest Neighbor Method.

FIGURE 1

Figure 1. Dendrogram (Nearest Neighbor Method, Squared Euclidean) generated from chemical characterizations of the supplements based on the macronutrients, micronutrients, organic matter, C/N ratio, and pH-values.

Supplements from the peanut and acerola juice waste showed the highest values of Fe and C/N ratio, and the peanut waste showed high Cu and Mn contents. The mix of supplements (33.3% peanut waste + 33.3% acerola juice waste + 33.3% noble grains) showed intermediate results, which were similar to the supplement formulated with the acerola juice waste, which had the highest proximity resulting in inferior distance in the Nearest Neighbor Method. The peanut waste supplement showed superior distance to the other supplements being the most different supplement from the chemical point of view when compared to the other supplements (Figure 1).

As the evaluation of the yield in the flushes were separately done, ABL 16/01 strain presented the highest results when the supplements were added, which can be checked comparing the yield values in each flush (1st, 2nd, 3rd, and 4th) with the other strains. In the substrate control, there was no significant difference among yield values in each flush by the strains, except the third flush (Table 3).

TABLE 3

Table 3. Results of yield in the 1st, 2nd, 3rd, and 4th flush, during the production phase of A. subrufescens cultivation.

Considering the 1st flush, the Pro Mycel Gold and peanut waste supplements provided the highest yields with ABL 16/01 strain. The substrate control provided the highest yield with ABL 16/02 strain, and ABL 16/03 strain showed no response to substrate supplementation. Although ABL 16/03 strain did not show a significant difference due to the supplementation, it was verified that Ca contents (21–25 g kg⁻¹) and B content (23–26 mg kg⁻¹) of the supplements positively and negatively influenced the yield values during the 1st flush (Table 5).

In the 2nd flush, the mix of supplement provided the highest yield with ABL 16/01. Once again, the substrate control provided the highest yield with ABL 02/16 strain, and ABL 16/03 strain showed no response to supplementation. Negative correlations were observed between the P (3.4–5.3 g kg⁻¹), K (14–17 g kg⁻¹), Mg (1.9–3.2 g kg⁻¹), and B (26 mg kg⁻¹) contents in the 2nd flush for ABL 16/02 and ABL 16/03 strains. The ABL 16/03 strain seems to be sensitive to the B contents of the supplements.

In the 3rd flush a particular results with the acerola juice waste provided the highest yield, significantly higher than control substrate in the three strains studied (Table 3), which may indicate a slow release of nutrients from this supplement to the mushroom, although correlation was not observed between any strains, chemical characteristics and 3rd flush (Table 5).

It is important to emphasize the influence of supplementation in the last flush (4th), to all stains used, when compared with the control. Some chemical characteristics may explain the positive contribution of the supplements in the high yield obtained: (i) the amount of Cu (close to 15 mg kg⁻¹), Fe (close to 795 mg kg⁻¹), and Mn (close to 52 mg kg⁻¹) for the ABL 16/01 strain; and (ii) the amount of S (close to 2.8 mg kg⁻¹) for the ABL 16/02 and the ABL 16/03 strain (Tables 2, 3).

The only strain that did not respond to supplementation in the total yield was the ABL 16/02, for which superior yield was observed with the substrate control (Table 4). The addition of acerola juice waste to the substrate cultivated with the ABL 16/01 strain resulted in a significant superior total yield due to the low P (1.8 g kg⁻¹), K (9 g kg⁻¹), and Mg (1.7 g kg⁻¹) contents, which directly negatively influences the number of mushrooms harvested (Table 5). The high values of the C/N ratio (26) provided an increase in the total yield for ABL 16/01 strain. The amount of Cu and Mn provided a positive correlation with the number of mushrooms for the ABL 16/01 strain. Finally, the ABL 16/03 strain responded to the addition of supplements with high N content, providing significant superior yield.

TABLE 4

Table 4. Results of total yield, number, and weight of mushroom, during the production phase of A. subrufescens cultivation.

TABLE 5

Table 5. Correlations between chemical characteristics of the supplements and the production parameters of the mushroom cultivation.

Although correlation found among the chemical characteristics of the substrates and the weight of the mushrooms, ABL 16/02 strain provided mushrooms with high mushroom weight, as well as Pro Mycel Gold ones (Table 4).

Discussion

The supplementation of the compost or substrate at spawning is an important and necessary practice used in A. bisporus and P. ostreatus cultivation to improve the quality of the mushroom and the efficiency of the crop during commercial production. Although supplements are not marketed around the world for the commercial production of A. subrufescens, upgrading the productive process can make a difference for the development of this important medicinal species.

Commercial supplements are marketed in different countries with a high potential for mushroom industry. Currently, the countries with higher mushroom production are China, USA, Poland, Netherlands, India, France, Spain, Canada, Mexico, and others (Royse et al., 2017). Some of these countries, like China and India, do not have companies that commercialize supplements to be applied in the substrate for mushroom production. In addition to these large mushroom-producing countries, other countries also produce mushrooms with a regular production scale, such as Brazil, Argentina, South Africa, Iran, Thailand, Vietnam, etc. Therefore, in our understanding, the practice of supplementation can also be performed in these countries using agricultural wastes or even noble grain meal.

In our literature review, two reports were found that utilized practice of substrate supplementation in the production of A. subrufescens (Kopytowski Filho et al., 2008; Dias et al., 2014). These studies had positive and negative results regarding the practice of supplementation. In both reports, the authors did not verify the influence of chemical characteristics of the supplements as a function of the physiological development of the mushrooms (1st, 2nd, 3rd, 4th, total yield, number, and weight of mushroom), beside, they did not use three different strains.

The present research confirms the importance of the supplementation practice, not just with commercial supplements but also with supplements based on agricultural wastes (peanut and acerola juice). The supplements based on noble grains may be used in some countries and have very similar chemical characterizations to the commercial supplements (Figure 1). The use of an appropriated strain is fundamental to supplementation practice. Subsequently, several companies that market supplements also market strains (i.e., Amycel and Lambert), providing greater safety in the production process.

The addition of acerola juice waste with the ABL 16/01 strain improved the total yield ~39%, and the addition of Pro Mycel Gold in the ABL 16/03 strain improved yield ~51% relative to the unsupplemented compost.

Due to the use of six different sources of organic supplements and three commercially grown strains in Brazil, it was possible to find some correlations that may be useful for the formulation or use of a waste as a substrate supplement to produce A. subrufescens. The most important elements that were verified in the two strains (ABL 16/01 and ABL 16/02) are P, K, and Mg, whose contents above 3.4, 14, and 1.9 g kg⁻¹ can reduce the yield of the mushrooms (in the flush analyzed separately or in total yield). Sinden in 1949 already warned the mushroom producers about the problem of Mg toxicity, at this time the approach was carried out in the correction of the casing layer pH using dolomitic limestone for A. bisporus cultivation (Atkins, 1974). Later Zied et al. (2012) verified the same negative effect of Mg using dolomitic limestone in A. subrufescens cultivation.

S content was also verified as an important macronutrient in two strains (ABL 16/02 and ABL 16/03) in the 4th flush, whose content close to 2.8 g kg⁻¹ provided high yield (Tables 2, 3). The use of S in the form of calcium sulfate (CaSO₄) is well-documented in the cultivation of mushrooms, being added as an ingredient in the preparation of substrate of the species Pleurotus spp., Lentunula edodes, A. bisporus in different amounts for improving the physical characteristics of the substrate and provide Ca and S for mushroom nutrition (Liyama et al., 1994; Curvetto et al., 2002; Mandeel et al., 2005; Uddin et al., 2013). The macronutrient values found in the correlation can be used as reference for future studies involving dose response of an element and yield of mushroom, i.e., increasing doses of S in the substrate (2.0, 2.4, 2.8, 3.2, 3.6 g kg⁻¹).

The B content also reduced the harvest in the 1st and 2nd flush in the ABL 03/16 strain. Ca, S, Cu, Fe, and Mn were found to contribute positively to the physiological development of the mushroom. Estrada Rodrigues and Royse (2007) also verified the positive effect of these micronutrients (Mn and Cu) when applied to the substrate on the yield of Pleurotus eryngii.

The N content and the C/N ratio provided different reactions depending on the strain used (Table 5). Some studies reported the influence of the N content and the C/N ratio in the production of the compost for A. subrufescens production (Zied and Minhoni, 2012; Llarena-Hernández et al., 2014; Pardo-Giménez et al., 2014). In Brazil, the compost used for A. subrufescens production has a C/N ratio close to 27/1 (at the end of Phase II), and in Europe, the compost has a C/N ratio close to 18/1 (at the end of Phase II) (Andrade et al., 2007; Siqueira et al., 2011; Zied et al., 2011b; Llarena-Hernández et al., 2013, 2014).

The difference in the C/N ratio used in the different continents is related to the method of preparation of the compost (formulation, Phase I, and Phase II). In Europe, the compost used in the production of A. subrufescens is the same as the compost prepared to A. bisporus production, and in Brazil, a poorer compost with a higher C/N ratio is used specifically for A. subrufescens production. In this sense, we can consider not only the method of preparation of the compost but also the nutritional and specific demand of the macro and micronutrient of the strain used. There are strains more demanding in N content and others in C content.

Finally, the composting method used to produce A. subrufescens is still not ideal, despite advances and the publication of new information. It is not even possible to obtain the highest yield in the first flush of the harvest. In the present manuscript, the highest yields were obtained in the 2nd (media of 6.54%) and 3rd flushes (media of 4.08%) (Table 3). Other authors have also verified the low yield in the 1st flush and the long cycle of crop (Zied and Minhoni, 2009; Colauto et al., 2011; Zied et al., 2011b; Pardo-Giménez et al., 2014; Martos et al., 2017).

Conclusion

The practice of supplementation is an important tool for improving yield in the industrial production of A. subrufescens. Waste materials and noble grains can be selected as quality supplements. The use of appropriated strains is essential to the success of the practice of supplementation. We suggest that materials with high Mg content should be avoided on the selection of an ideal supplement, while materials with high S, Cu, and Mn contents should be selected as ideal supplements. Therefore, other studies should be performed to better understand this relationship in an experimental crop, to know, with safety, which macro and micronutrients should be present in a commercial supplement to be used in large scale by the mushroom industry.

Author Contributions

DZ assisted in the experimental design, supervised the execution and the interpretation of the data, CC and MZ carried out the experiments, JP analyzed the results, ED and AP-G coordinated the statistical and wrote the manuscript. All authors read and approved the final manuscript.

Funding

This research was supported financially by Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP 15/15306-3 and 15/24788-1).

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

The authors are grateful to Centro de Estudos de Cogumelos (CECOG) and the Universidade Estadual Paulista (UNESP) for providing an adequate support for conducting the study and for Funghi & Flora company for providing the commercial strains.

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