Enhancing Pleurotus ostreatus P. Kumm cultivation on peel of the fruit of Astrocaryum aculeatum (Jacq.) G. Mey by investigating the influence of moisture and supplementation with wheat bran

Melhorando o cultivo de Pleurotus ostreatus (Jacq.) P. Kumm na casca do tucumã (fruto de Astrocaryum aculeatum) por meio da avaliação da influência da umidade e de suplementação com farelo de trigo

Abstract

This study investigates the impact of moisture and wheat bran supplementation on the biological efficiency (BE) and nutritional profile of Pleurotus ostreatus (Jacq.) P. Kumm cultivated on peels of Astrocaryum aculeatum G. Mey. Utilizing a factorial design, variations in substrate composition were systematically analyzed to determine optimal conditions for mushroom yield. The methodology encompassed strain acquisition, spawn and substrate preparation, fruiting induction, biological efficiency calculation, and chemical composition analysis of both substrate and mushrooms. Results highlighted a significant variance in BE across different levels of moisture and bran supplementation, with the highest BE (45.6%) observed at 50% moisture and 5% bran supplementation. Statistical analysis revealed that both factors, individually and interactively, significantly influence BE. The chemical analysis of mushrooms showcased a nutritious profile, emphasizing the potential of this cultivation approach for producing high-value food sources. The findings contribute to the understanding of substrate optimization for mushroom cultivation, and provides information on sustainable agricultural practices and food security.

Keywords:
biological efficiency; wheat bran supplementation; moisture level; substrate optimization; mushroom cultivation

Resumo

Este estudo investiga o impacto da umidade e da suplementação com farelo de trigo na eficiência biológica (EB) e no perfil nutricional de Pleurotus ostreatus (Jacq.) P. Kumm cultivado em casca de tucumã, como é conhecido o fruto do tucumãzeiro (Astrocaryum aculeatum G. Mey). Utilizando um planejamento fatorial, as variações na composição do substrato foram sistematicamente analisadas para determinar as condições ideais para a produção de cogumelos. A metodologia abrangeu aquisição de cepas, preparação de semente e substrato, indução de frutificação, cálculo de eficiência biológica e análise de composição química de substrato e cogumelos. Os resultados destacaram uma variação significativa no EB entre diferentes níveis de umidade e suplementação de farelo, com o EB mais alto (45,6%) observado com 50% de umidade e 5% de suplementação de farelo. A análise estatística revelou que ambos os fatores, individual e interativamente, influenciam significativamente o EB. A análise química dos cogumelos apresentou um perfil nutritivo, enfatizando o potencial desta abordagem de cultivo para a produção de fontes alimentares de alto valor. As descobertas contribuem para a compreensão da otimização de substratos para o cultivo de cogumelos, oferecendo insights sobre práticas agrícolas sustentáveis ​​e segurança alimentar.

Palavras-chave:
eficiência biológica; suplementação com farelo de trigo; teor de umidade; otimização de substrato; cultivo de cogumelos

1. Introduction

The mushroom Pleurotus ostreatus, commonly known as the oyster mushroom, hiratake, shimeji, or houbitake, has been extensively studied and cultivated in various parts of the world (Sales-Campos et al., 2021; Abou Fayssal et al., 2021; Ejigu et al., 2022; De et al., 2023). Due to its nutritional profile which is rich in proteins, metabolizable carbohydrates, and fibers, while being low in lipids and calories, it is considered an important food source (Mahfuz et al., 2020; Vishwakarma et al., 2017). In addition to its nutritional value, species of Pleurotus are well-known for their edible, medicinal, enzymatic, and adaptive properties, effectively utilizing a wide range of agro-industrial by-products (Ghafoor and Niazi, 2024).

The use of agricultural by-products for the cultivation of edible fungi presents a sustainable avenue for waste valorization and the production of nutritious food sources. A. aculeatum, a palm species indigenous to the Amazon region, bears fruits whose peels (epicarp) are generally discarded after consumption or processing, contributing to agricultural waste (Obodai et al., 2003; Ritota and Manzi, 2019; Pereira et al., 2022). The proximate composition of these by-products, including moisture, protein, fat, ash, and fiber content, is crucial for evaluating their potential as substrates in mushroom cultivation (Ritota and Manzi, 2019; Obodai et al., 2003; Bellettini et al., 2019; Bandura et al., 2022).

Previous research has primarily focused on the use of conventional substrates like straw and wood chips for mushroom cultivation, with limited exploration into the use of tropical fruit peels (Bellettini et al., 2019; Thongklang and Luangharn, 2016; Raman et al., 2020). The tucumã (A. aculeatum) fruit peel has potential for sustainable mushroom production. Studies have shown that the nutritional content of a substrate significantly affects the biological efficiency of mushroom cultivation, a measure of the mushroom yield based on the dry weight of the substrate used (Barbosa et al., 2009; Santos et al., 2022). However, the influence of moisture content and supplementation with wheat bran on the biological efficiency of mushrooms cultivated on the peel of tucumã has not been investigated. This gap in knowledge hampers the optimization of substrate formulations for maximizing yield and nutritional content of the produced mushrooms.

Regionally, there exists a significant gap in scientific literature regarding the valorization of by-products (Barbosa et al., 2009; Yuyama et al., 2008; Didonet and Ferraz, 2014; Matos et al., 2019). The Amazon basin warrants specific studies to explore the suitability and efficiency of local agricultural wastes as substrates. The tucumã fruit peel represents a regionally abundant resource that, if effectively utilized, could contribute to the circular economy and promote sustainable agricultural practices in the Amazon (Barbosa et al., 2009; Didonet and Ferraz, 2014; Azevedo et al., 2017; Matos et al., 2019; Yuyama et al., 2008).

The relevance of this investigation lies in its potential to contribute to sustainable agriculture and food security in the Amazon region. This research delves into three pivotal scientific inquiries. First, we determined the centesimal (proximate) composition of tucumã (A. vulgare) fruit peel (epicarp), which is crucial for assessing its viability as a substrate for mushroom cultivation. Second, we investigated the influence of moisture content and the supplementation of wheat bran on the biological efficiency of mushrooms produced using tucumã fruit peel as the primary substrate, a factor that significantly impacts the yield and quality of the mushrooms. And third, we analyzed the centesimal composition of the mushrooms cultivated on this substrate, to evaluate their nutritional value.

2. Materials and Methods

2.1. Pleurotus ostreatus

A commercial strain identified as P. ostreatus (Jacq.) P. Kumm Gumelos 1 from (Gumelos®, Brazil) (Shopee, 2024), acquired in July 2020, was utilized for this study. This strain has been preserved in the Collection of Medically Relevant Microorganisms at INPA. Cultivation involved mycelium fragments on petri dishes containing yeast extract-peptone-dextrose agar (YPD) medium, incubated at 25 °C for 7 days in a Panasonic® MIR-154, (Osaka, Japan) incubator.

2.2. Peel of Astrocaryum aculeatum

The peels of A. aculeatum, an agro-industrial residue, were collected from open markets in Manaus in April 2020. Following collection, the peels were subjected to aseptic treatment with a 0.03% chlorine solution for 15 minutes, dried at 70 °C for 48-72 hours, and ground using a blender model LI2 (Skymsen®, Brusque, Brazil). The particle size was standardized between 1-5 mm and stored in conditions that maintained their integrity until use.

2.3. Wheat seeds and wheat bran (substrate supplement)

The wheat seeds used to prepare the inoculum were sourced from Bunge Alimentos S.A. (Bunge Alimentos S.A., São Paulo, Brazil), while the wheat bran used to supplement the substrate was sourced from Moinho Globo® (Moinho Globo, Sertanópolis, Brazil). This wheat bran was standardized to a granularity of 1-5 mm. The proximate composition of the bran was as follows: moisture content 13.5%, crude protein 15.5%, crude fiber 11.0%, crude fat 4.0%, and ash 5.5%. Wheat bran is used as a supplement in the production of laccase mainly due to its nutritional content, affordable cost and ability to stimulate enzyme production and mushroom growth.

2.4. Proximate composition of the A. aculeatum fruit peel and oyster mushrooms cultivated utilizing peel of the fruit of Tucumã

The proximate composition of the peel of the fruit of A. aculeatum and Oyster mushrooms, including protein, lipids, ash, moisture, and carbohydrate content, was determined according to the standard methodologies prescribed by the Adolfo Lutz Institute (IAL, 2008). Further details of these analyses are presented in the Analytical Assays section.

2.5. Optimal moisture and wheat bran supplementation percentages for maximizing biological efficiency (BE)

2.5.1. Inoculum preparation

In the initial phase of the experiment, wheat grains designated for spawn preparation underwent a rigorous cleaning process, involving thorough washing and soaking in filtered water for 12 hours. Once dried, 30 grams of these grains were placed into 125 mL Erlenmeyer flasks, sealed with cotton plugs, and sterilized at 121 °C for 0.75 hours under 1.1 atm pressure. Subsequently, for mycelial inoculation, six 1 cm diameter mycelium plugs, pre-cultivated on petri dishes, were transferred aseptically into the flasks within a laminar flow hood (ESCO® model AC2-4S3). These inoculated flasks were then incubated in a Panasonic® model MIR-154 incubator for 14 days to promote mycelial proliferation (Urben, 2017).

2.5.2. Bioprocess description

The processed substrates were then subjected to moisture adjustment and supplemented with bran to enhance nutrient availability. Each batch, consisting of 400 g of substrate, was packed into autoclavable HDPE bags (Embrasil Embalagens Plásticas Ltda., São Paulo, Brazil). Sterilization of the substrates was achieved through two autoclave cycles (30 minutes at 121 °C and 1.1 atm pressure) with a 24-hour interval between cycles to ensure complete sterilization and (Mazaro et al., 2007).

2.5.3. Incubation process

Following sterilization, the substrate bags were inoculated with 30 grams of the prepared mycelium spawn under sterile conditions within a laminar flow hood. The inoculated substrates were then transferred to a BOD chamber (Quimis® model Q315M25, São Paulo, Brazil) set at a controlled temperature of 25 °C.

2.5.4. Fruiting

Once complete mycelial development was observed (around 25 days), the bioreactors were exposed to a temperature of 18 °C where, after 48 hours, the initiation of primordia formation was observed. The bags were then opened and transferred to a room illuminated with fluorescent light (8-10 hours/day), with relative moisture increased using a household humidifier (Springer® model ISHD-0033) inserted in the BOD chamber (Quiñones-Muñoz et al., 2018).

2.5.5. Factorial design

The factorial design employed to determine the optimal moisture and wheat bran supplementation percentages for maximizing biological efficiency (BE) involved a 2² design with replication at the central point, as previous described (Barros Neto et al., 1995). Moisture and wheat bran supplementation were identified as critical factors, with biological efficiency, defined as the quantity of mushrooms produced, serving as the response variable. The statistical significance of these factors was determined through linear equation modeling and validated by Analysis of Variance (ANOVA). The response surface was designed using the model obtained. The detailed explanation of biological efficiency (BE) measurements will be provided in the Analytical Assays section.

2.6. Analytical assays

2.6.1. Proximate composition

The chemical composition of the substrates and mushrooms was analyzed using standard protocols from the Physicochemical Methods for Food Analysis by the Adolfo Lutz Institute (IAL, 2008). Moisture content was determined through gravimetric drying in a precision oven (Memmert GmbH + Co. KG, Schwabach, Germany) at 105 °C ± 2 °C until constant weight. Ash content was assessed by incinerating 2 g of dried sample at 550 °C for 6 hours in a muffle furnace (Thermo Fisher Scientific, Waltham, MA, USA) to completely remove any organic material. Protein content was measured via Kjeldahl distillation (Buchi Labortechnik AG, Flawil, Switzerland), applying a nitrogen-to-protein conversion factor of 6.25 for the mushrooms and 5.71 for the substrates, following digestion with concentrated sulfuric acid (≥ 95%, Sigma-Aldrich, St. Louis, MO, USA). Lipid content was determined via Soxhlet extraction (Gerhardt GmbH & Co., Königswinter, Germany), using petroleum ether (Sigma-Aldrich, purity ≥ 99%) with 8 hours reflux time. The total carbohydrate content was calculated by the difference, adding the values of moisture, ash, protein and lipids, and subtracting the total from 100%. Each assay was performed in triplicate (n=3), with the results reported as mean ± standard deviation to ensure precision and reproducibility.

2.6.2. Biological efficiency

Biological efficiency (BE) was calculated to assess the yield of mushroom fruiting bodies. After harvesting, the fruiting bodies were weighed, and BE was determined using the following Equation 1:

$$BE\left(\%\right)=\left(\begin{array}{l}Massoffreshmushrooms\left(g\right)\\ Drysubstratemass\left(g\right)\end{array}\right)\times 100$$ (1)

This calculation follows the standard methodology (Thongklang and Luangharn, 2016; Santos et al., 2022), where the efficiency of mushroom production is directly related to the substrate utilized.

2.7. Statistical analysis

Statistical analysis was performed using STATGRAPHICS® 9 software. The experiments were conducted in triplicate, and the results were analyzed through ANOVA with a 95% confidence interval to assess the impact of the variables on biological efficiency and laccase activity.

3. Results

3.1. Proximate composition of the A. aculeatum fruit peel

Employing standard analytical methods, we quantified the components, including ash, protein, lipids, carbohydrates, and moisture content (Figure 1). Our findings reveal a composition: 2.7 ± 0.1% ash, 9.8 ± 0.1% protein, 25.2 ± 0.3% lipids and 61.1 ± 0.6% carbohydrates (on a dry weight basis).

Figure 1
Peel of Tucumã Fruit (Astrocaryum vulgare) Used as a Substrate for Pleurotus ostreatus Cultivation: (a) In natura Husk; (b) Dried Husk; (c) Ground Husk”.

3.2. Optimal moisture and wheat bran supplementation percentages for maximizing biological efficiency (BE)

In our investigation into the influence of substrate composition in maximizing the biological efficiency (BE) of P. ostreatus cultivated on A. aculeatum peel, a 2² factorial design revealed significant variances in mushroom yield across different moisture and wheat bran supplementation levels (Table 1).

Table 1
Factorial Design 2² Analysis with Central Point Replication for Optimizing Moisture and Wheat Bran Supplementation in P. ostreatus Cultivation on Astrocaryum aculeatum Peel.

Moisture level (%)	Bran suplementation (%)	BE (%)
60	10	19
70	15	20.6
50	15	28
70	5	0
50	5	45.6
60	10	16.7
60	10	20

• BE = biological efficiency.

The empirical data, summarized in Table 1, indicated a pronounced peak in biological efficiency at a moisture content of 50% and wheat bran supplementation of 5%, where BE reached 45.6%. Conversely, a supplementation of 5% at 70% moisture level resulted in lower BE of 0%, underscoring the sensitivity of P. ostreatus yield to substrate conditions.

Pareto analysis indicated statistical significance of both moisture level and bran supplementation on the biological efficiency (BE) of P. ostreatus cultivation, as well as their combined effect. The negative coefficients for moisture level (-3.175) and bran supplementation (-10.95) suggest that an increase in these factors individually decreases the BE. However, the positive coefficient for the interaction term (0.185) indicates a combined positive effect on BE when both factors are increased together. The derived linear equation from the data (Table 1) is (Equation 2):

$$\begin{array}{l}BE=210.14-3.17\times MoistureLevel-10.95\times \\ BranSupplementation+0.185\times \\ \left(MoistureLevel\times BranSupplementation\right)\end{array}$$ (2)

This mathematical model demonstrates a statistically significant regression for both the main effects (moisture level and bran supplementation) and their interaction, with a high R² value indicating a good model fit. The p-value for moisture level was 0.0061, indicating that the moisture level had a statistically significant effect on BE. The p-value for bran supplementation was 0.0217, showing that bran supplementation also significantly affects BE. The interaction between moisture level and bran supplementation has a p-value of 0.0202, indicating that the interaction effect was statistically significant (Figure 2).

Figure 2
Response surface (Matplotlib, 2024) resulted from Equation 1: Influence of Moisture (%) and Wheat Bran Supplementation (%) on the Biological Efficiency of P. ostreatus Cultivation on Astrocaryum aculeatum Peel.

The model has an R² value was 0.9543, indicating that approximately 95.43% of the variation in biological efficiency (BE) can be explained by the model. This high R² value suggests a strong fit between the model and the observed data.

3.3. Proximate composition of the oyster mushrooms cultivated utilizing tucumã (A. aculeatum) peel

Upon examination of the centesimal composition of oyster mushrooms cultivated utilizing tucumã peel. The evaluation per 100g of the fresh mushroom sample demonstrated a moisture content of 66.45% with a standard deviation (SD) of ±0.17%, ash at 2.03% (SD ±0.01%), protein at 4.69% (SD ±0.05%), lipids at 5.65% (SD ±0.06%), and carbohydrates constituting 21.18%, illustrating the mushrooms’ nutritional profile (Figure 3). The protein content in the dry matter of the mushroom is calculated to be approximately 13.98%, while the carbohydrate content in the dry matter is approximately 63.13%.

Figure 3
Enhancing Pleurotus ostreatus Yield through Moisture Regulation and Wheat Bran Enrichment on Tucumã Peel Substrate”. (a) Colonized Tucumã Peel Residue; (b) Primordia Formation; (c, d, e) Fruit Body Development Stages; (f) Post-Harvest Tucumã Peel Mushroom Residue.

4. Discussion

Our investigation into the potential of peel of the fruit of A. aculeatum as a substrate for P. ostreatus cultivation has yielded promising results. The proximate analysis of the substrate revealed a notable composition conducive to mushroom cultivation, specifically, high carbohydrate and protein content. These findings align closely with our initial hypotheses, suggesting that the peel of tucumã fruit possesses the necessary nutritional components to support fungal growth.

The centesimal composition of peel of the fruit of A. aculeatum is a composition of 2.7% ash, 9.8% protein, 25.2% lipids, and 61.1% carbohydrates. Our results agree with studies conducted by Matos et al. (2019) which highlight the substantial lipid and carbohydrate content within the tucumã peel. The consistency with existing literature validates our analytical approaches and confirms the peel’s suitability as a substrate for mushroom cultivation (Santos et al., 2022).

The influence of moisture content and wheat bran supplementation on the biological efficiency of P. ostreatus was profound. Optimal conditions were identified at 50% moisture and 5% wheat bran supplementation, leading to a maximum biological efficiency of 45.6%. This optimal combination underscores the critical role of precise substrate conditioning in mushroom cultivation. Previous studies highlight the importance of substrate moisture content and nutritional supplementation for fungal growth (Bellettini et al., 2019; Ritota and Manzi, 2019; Raman et al., 2020; Alsanad et al., 2021; Pereira et al., 2022; Bandura et al., 2022). Our findings (EB 45%) not only corroborate these earlier observations but also underscore the effectiveness of tucumã peel as a novel substrate, demonstrating its potential to support high-yield mushroom cultivation. Values of EB considered good for P. ostreatus in the literature typically range between 50% and 100%, with values above 70% frequently cited as indicative of efficient production. However, further biochemical process optimization is necessary to enhance the efficiency and sustainability of P. ostreatus production on this substrate (Sales-Campos, 2010; Karp et al., 2012; Thongklang and Luangharn, 2016; Pereira et al., 2022; Bandura et al., 2022).

The proximate composition of P. ostreatus mushrooms cultivated on the tucumã peel substrate revealed a distinct nutritional profile that diverges from prior research findings (Sales-Campos 2010; Thongklang and Luangharn, 2016; Membrillo et al., 2011; Pereira et al., 2022). The observed concentrations of protein (13.98% dry weight) and carbohydrates (63.13% dry weight) are notable, but what stands out is the high lipid content (16.85% dry weight). Generally, P. ostreatus mushrooms have a protein content ranging from 15% to 25% dry weight, carbohydrate content between 50% and 60% dry weight, and lipid content of about 2% to 4% dry weight (Pereira et al., 2022; Bandura et al., 2022). The substrate’s rich lipid environment likely influenced the mushrooms’ nutrient profile, resulting in higher lipid content and relatively lower protein concentration.

Despite our encouraging findings, this study acknowledges limitations, such as the narrow range of experimental conditions and the singular method of mushroom cultivation in bags. Future research should expand the factorial design to explore a broader spectrum of conditions and incorporate alternative cultivation methods. Nonetheless, our study makes significant contributions to the fields of science and technology, particularly in the context of Amazonian bio-industry development. By demonstrating the viability of tucumã peel as a substrate for mushroom cultivation, we highlight a sustainable approach to waste utilization that could bolster food security and contribute to the circular economy in the Amazon region.

5. Conclusion

This study demonstrated the potential of tucumã (Astrocaryum vulgare Mart.) fruit peel as a substrate for Pleurotus ostreatus (strain Gumelos 1) cultivation. Key findings include:

• Proximate Composition: Tucumã peel showed high carbohydrate (61.1%) and protein (9.8%) content, confirming its suitability for mushroom cultivation;

• Optimal Cultivation Conditions: Maximum biological efficiency (BE) of 45.6% was achieved with 50% moisture and 5% wheat bran supplementation, emphasizing the importance of substrate preparation for yield and quality;

• Nutritional Profile of Mushrooms: Pleurotus ostreatus grown on tucumã peel displayed a unique nutritional profile, including higher lipid content (16.85%) than usual, influenced by the substrate’s lipid-rich composition.

Availability of data and material

The data that support the findings of this study are available within the article.

Acknowledgements

We gratefully acknowledge the financial support from FAPEAM (Fundação de Amparo à Pesquisa do Estado do Amazonas), CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico), and CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), under Process Number 062.00898/2019. The project, titled “Production, Stability, and Applicability of Colorants Produced by Filamentous Fungi Isolated from Soil Samples of the Amazon Region,” was funded by the EDITAL N. 006/2019 - UNIVERSAL AMAZONAS. The project was coordinated by João Vicente Braga de Souza.

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Publication Dates

• Publication in this collection
  14 Mar 2025
• Date of issue
  2025

History

• Received
  12 July 2024
• Accepted
  02 Dec 2024