Carbon-to-nitrogen ratios for Agaricus brasiliensis on the axenic method

Relação carbono/nitrogênio do substrato pelo método de cultivo axênico para Agaricus brasiliensis

PRODUÇÃO VEGETAL

Carbon-to-nitrogen ratios for Agaricus brasiliensis on the axenic method

Relação carbono/nitrogênio do substrato pelo método de cultivo axênico para Agaricus brasiliensis

Lienine Luiz Zaghi Junior; Giani Andrea Linde; Nelson Barros Colauto^*

Instituto de Ciências Exatas, Agrárias, Tecnológicas e Geociências, Universidade Paranaense, Praça Mascarenhas de Moraes 4282, Cx. Postal 224, 87502-210, Umuarama, Paraná, Brazil

ABSTRACT

Cultivation techniques for Agaricus brasiliensis (composting method) and substratum formulations are the same ones used for Agaricus bisporus. Most of the carbon-to-nitrogen (C:N) ratios reported for A. brasiliensis are similar to those used for A. bisporus on the composting method and there are few studies about the variation of C:N ratios for A. brasilienses on the axenic method. The objective of this study was to verify the mycelial growth of A . brasiliensis on different C:N ratios using regional by-products as substrate formulation on the axenic method. Studied C:N ratios of substrate (mixture of soybean and cassava fibers) ranged from 11:1 to 248:1, with nitrogen content ranging from 4.25 to 0.20%, respectively. It was concluded that substrate with only soybean fiber generates higher mycelial growth than any formulation with cassava fiber; the highest mycelial growth on substrate is with C:N ratio of 11:1 (N = 4.25%); the intermediate growth is with C:N ratio range from 15:1 to 50:1 (N from 3.31 to 0.98%); and the lowest growth is with C:N ratio of 100:1 or higher (N < 0.50%).

Key words: Agaricus blazei, mycelial growth, substrate, cultivation.

RESUMO

As técnicas de cultivo do Agaricus brasiliensis (método de compostagem) e formulação de substrato são as mesmas utilizadas para o Agaricus bisporus. A maioria das relações carbono/nitrogênio (C/N) relatadas para A . brasiliensis são similares às usadas para A. bisporus no método de compostagem. Há poucos estudos sobre a variação da relação C/N para A. brasilienses para o método axênico. O objetivo deste trabalho foi verificar o efeito de diferentes relações C/N no crescimento micelial de Agaricus brasiliensis utilizando subprodutos regionais como substrato pelo método axênico. As relações C/N no substrato (misturas de fibra de soja e de mandioca) estudadas variaram de 11 a 248 com consequentes concentrações de nitrogênio de 4,25 a 0,20%, respectivamente. Concluiu-se que os substratos somente com fibra de soja propiciam maior crescimento micelial que qualquer mistura com fibra de mandioca; o crescimento micelial é maior no substrato com relação C/N de 11 (N = 4,25%), intermediário na faixa de relação C/N entre 15 e 50 (N = 3,31 e 0,98%) e menor na relação C/N de 100 ou superior (N < 0,50%).

Palavras-chave: Agaricus blazei, crescimento micelial, substrato, cultivo.

Introduction

Agaricus brasiliensis Wasser et al. (A. blazei Murrill sensu Heinemann), (WASSER et al., 2002), also denoted A. subrufescens (KERRIGAN, 2005), is a fungus native to Brazil (BRAGA et al., 1998; COLAUTO et al., 2002; DIAS et al., 2004; EIRA, 2003; WASSER et al., 2002) and it has been reported many therapeutic properties (KIM et al., 2005; KIMURA et al., 2004; MIZUNO, 2002; OSHIMAN et al., 2002; RODRIGUES et al., 2003; SOUZA-PACCOLA et al., 2004). It has been produced in Brazil for commercial purposes since 1990 and 90% of its current production is exported to Japan (EIRA, 2003). The A. brasiliensis cultivation techniques (composting method) and substratum formulations are the same ones used for Agaricus bisporus (BRAGA et al., 1998; SÁNCHEZ, 2004). However, because A. brasiliensis is a fungus from tropical origin, the cultivation techniques need to be adapted to its own characteristics (EIRA, 2003; MANTOVANI et al., 2007). One of the most important aspects for a good mycelial growth is the substratum source, which directly affects the bioconversion ability of raw material and consequently the productivity. It is important as well to develop a substratum formulation from available local organic sources, fully taking advantage of regional by-products (EIRA et al., 2005), and also reducing transportation costs (DIAS et al., 2004).

Brazil is one of the biggest producers of soybean (Glycine max) and cassava (Manihot esculenta). In 2006, the national production of soybean and cassava was, respectively, more than 52 and 26 million tons (IBGE, 2007). Soybean and cassava fibers resulting from industrialization process are generally used as animal feed, burned or dumped on the soil, increasing environmental damages associated to agricultural and industrial activities in Brazil (LEONEL et al., 1999). These by-products could be a sustainable alternate method to reduce environmental pollution and aggregate value as components of a substratum for A. brasiliensis.

Soybean and cassava fibers present different nitrogen (N) content. The excess or lack of N content in the substrate may be a limiting factor to fungus growth (CARLILE; WATKINSON, 1995). According to Rajarathnam and Bano (1989) there is a reduction of substratum degradation when N is excessively added. There is also a great variation of N content and carbon-to-nitrogen (C:N) ratios in substrate from agricultural or agro industrial by-products. A C:N ratio of 20:1 is related as suitable for most fungi (CHANG; MILES, 1989). For Agaricus bisporus C:N ratio variation is from 15:1 to 17:1 (MACCANNA, 1984), for Pleurotusfabellatus is from 30:1 to 117:1 (SRIVASTAVA; BANO, 1970), for Pleurotus tuber-regium is from 18:1 to 36:1 (WU et al., 2004), for Pleurotus ostreatus is around 85:1 (RAJARATHNAM; BANO, 1989), for Ganoderma lucidum is from 70:1 to 80:1 (HSIEH; YANG, 2004) and for Lentinula edodes is around 25:1 (OEI, 1996). Although research is extensive and advanced for several of these fungi, there is no studies of nitrogen sources or optimal range of C:N ratios use on axenic method for A. brasiliensis. Most of C:N ratios reported for A. brasiliensis are similar to those used for A. bisporus on composting method (ANDRADE et al., 2007; BRAGA et al., 1998; DONINI et al., 2006; EIRA, 2003; EIRA et al., 2005; KOPYTOWSKI FILHO; MINHONI, 2003). However Mantovani et al. (2007) have reported a study about variation of C:N ratios for A. brasilienses with mineral nitrogen sources on axenic method.

The axenic method is considered expensive because the substratum has to be sterilized but it was not found any report comparing the feasibility of axenic and composting method for A. brasiliensis cultivation. Most disadvantages on composting method are considered advantages on the axenic method. It is because the composting method is often empiric and presents handling difficulties like process standardization and control in relation to material during composting process (HERNANDEZ et al., 2003); need of ammonium neutralization after pasteurization (VAN GRIENSVEN, 1988) and damages by Sciaridae larvae (EIRA et al., 2005; MENZEL et al., 2003). Thus other alternate methods, which are more efficient, inexpensive, standardized and simplified for preparing the substratum formulation, should be studied in order to optimize A. brasiliensis production in Paraná State, Brazil.

Considering the limited knowledge of the A. brasiliensis cultivation techniques, generally adapted from A. bisporus cultivation technique (BRAGA et al., 1998), the objective of this study was to verify the mycelial growth of A. brasiliensis on different C:N ratios using regional by-products as substratum formulation on the axenic method.

Material and methods

This experiment was carried out in the Molecular Biology Laboratory of the Paranaense University (UNIPAR), Campus I of Umuarama, Parana State, Brazil. Agaricus brasiliensis ABL97/11 strain from the Molecular Biology Laboratory Fungus Collection of UNIPAR was used. The fungus was kept at 20ºC on solid malt extract medium (24 g L^-1), cut, and transferred to 90 mm Petri dishes with the solid malt extract medium -MEA- (45 g L^-1), and incubated in the dark at 28ºC. After that, three dishes were selected to inoculate all experimental treatments.

Soybean and cassava fibers were used as raw materials for substratum formulation (culture media). Dried soybean fiber was provided by Solae do Brazil. Cassava fiber was obtained from tubercles that were peeled, washed and grounded in a mixer. The obtained mass was transferred to a fabric filter and washed until the washing water was completely clear. The resulting cassava fiber was dried with air circulation at 45ºC for 10h. Both fibers were grounded in a mixer, sieved until granules were smaller than 355 pm, and kept in a freezer at -70ºC.

Both fibers were analyzed for moisture content at 105 ºC, total nitrogen content (Kjeldahl's method), and ash content at 550ºC (LARA et al., 1976). All determinations were performed in triplicate. C:N ratios were calculated according to Gerrits (1988), considering the carbon content to be 50% of the organic matter (total dried mass minus ash content multiplied by 0.5). From these data, substrate used in the treatments were compound of 30 g of fiber mixture and 15 g of agar per liter of distilled water in order to achieve each C:N ratio desired. Substratum made of malt extract agar (45 g L-¹) and only agar (15 g L-¹) was used as positive and negative controls, respectively. Each substratum was sterilized in autoclave at 121 ºC for 20 min. After that pH was adjusted to 6 using NaOH or HCl solutions which had previously been sterilized by filtration (0.22 µm pore size filter). All treatments were quadrupled.

Substrate containing fiber mixtures and positive and negative controls were inoculated with five millimeter diameter cylinders taken from the peripherical area of the fungal growth on MEA. Inoculum was placed in the middle of each Petri dish (treatment) and special care was taken to keep the cylinder mycelium in direct contact with each substrate. All steps of the experiment were carried out under aseptic conditions in a laminar flow chamber. Inoculated dishes were randomly arranged for mycelia growth in a chamber with air circulation and controlled temperature at 28.0ºC ± 0.1ºC.

For each replication, the mycelial growth was verified by calculating the average of four different measurements of the diameter (in mm) 17 days after inoculation. Four replications were made to calculate the mycelial growth diameter average for each treatment. Obtained data were evaluated using variance analysis and significant differences were determined by Tukey's test with a significance level of p < 0.05. Levels of mycelial density among the treatments were compared visually and registered at the end of the experiment.

Results and discussion

The analysis results of the soybean fiber, N and ash dry matter contents were 4.25 and 3.41%, respectively; for cassava fiber, 0.20 and 0.75%; and for MEA medium, 2.90 and 4.07%. Substratum formulations with these regional by-products were prepared based on these results (Table 1). Based on that MEA culture medium was calculated with C:N ratio of 17:1 and agar medium was considered inert to all treatments and with a estimated C:N ratio of 500:1.

A. brasiliensis presented three significantly (p < 0.05) different growing groups in function of C:N ratio and N content (Fig. 1). The maximum mycelial growth was obtained on the substratum formulation with soybean fiber only (C:N = 11:1; N = 4.25%), however, this fungus, apparently, can grow in higher N contents, as reported by Mantovani et al. (2007), which were not tested in this study because of the natural N limitation presented in the fibers used. In substratum formulations with C:N ratios that ranged from 15:1 to 100:1 (N from 3.31 to 0.50%) mycelial growth was constant, with no significant (p < 0.05) difference. However there was a lower mycelial growth in substratum formulations with C:N ratios higher than 100:1 (N < 0.50%). In the substrate with C:N ratio of 15:1 (about 23% of cassava and 77% of soybean fiber; Fig. 1) there was a significant (p < 0.05) reduction of the mycelial growth when compared to the substrate with C:N ratio of 11:1 (100% of soybean fiber). This may not be related just to N content difference. We suppose that cassava fiber may contain fungus growth inhibiting compounds even after autoclaving. On the other hand, the higher mycelial growth in the substratum formulation with soybean fiber only may be related to polysaccharides composition, mainly arabinogalactanes, whereas cassava fiber contains mostly starch and cellulose (LEONEL et al., 1999). Besides, soybean fiber is more porous and has higher water absorption capacity, approximately 10 g of water for each gram of fiber, whereas cassava fiber has 4 g of water for each gram of fiber (LINDE; MACHADO, 2001), providing a better enzymatic access and higher nutrient absorption to mycelial growth. Thus, the soybean fiber structure and the composition of protein and polysaccharides, associated to a higher N content, provided a more appropriate substrate to the development of A. brasiliensis.

The A. brasiliensis mycelial gowth ability to the higher N content in the substratum (C:N = 11:1; Figure 1) was not expected and it was higher than to other fungi like Agaricus bisporus (BRAGA et al., 1998; MACCANNA, 1984; VAN GRIENSVEN, 1988; ZHEN et al., 1995), Lentinula edodes (OEI, 1996; ROSSI et al., 2003), Ganoderma lucidum (HSIEH; YANG, 2004), Pleurotus ostreatus (RAJARATHNAM; BANO, 1989) and Pleurotus tuber-regium (WU et al., 2004). According to Maccanna (1984) it is recommended to Agaricus bisporus, when compost is used as substratum, a C:N ratio from 15:1 to 17:1, against a C:N ratio of 11:1 (N = 4.25%) to A. brasiliensis found in this study on axenic method. This capacity to use substrate containing high N contents is an advantage to A. brasiliensis, since high N contents can inhibit mycelial growth of other basidiomycete by repressing lignin degradation (KAMRA; ZADRAZIL, 1986). According to Macaya-Lizano (1988) substrate with high N contents and, consequently, low C:N ratios, did not provide the total substratum colonization and did not allow appropriate basidiocarp production for Pleurotus spp. Rajarathnam and Bano (1989) reported similar data, in which high N contents caused the increase of toxic substances in the culture medium, limiting the mycelial development and, consequently, basidiocarp production. However, A. brasiliensis was capable of keeping the vegetative growth with a high N contents (C:N = 11:1, N 4.25%; Figure 1), probably due to lignocellulolytic activity maintenance or yet the use of alternate enzymatic routes to keep carbon and nitrogen availability, suggesting that it is not a limitation for basidiocarp production. Zadrazil (1980) reported a relationship among basidiocarp protein content and its nutritional necessity and nitrogen availability in the substrate. This higher N metabolization capacity of A. brasiliensis, mainly when compared to A. bisporus, can be supported by the higher protein content in the basidiocarp, approximately 40% in dry matter (BRAGA et al., 1998). Other mushrooms, for instance, present inferior amounts of proteins in dry matter: Pleurotus ostreatus (30.4%), Agaricus bisporus (23.9%), Volvariella volvacea (21.2%), Flammulina velutipes (17.6%) and Lentinula edodes (13.4%) (MILES; CHANG, 1997).

Eira et al. (2005) reported that A. brasiliensis production, on composting cultivation method, with C:N ratio of 17:1, was lower due to the increase of the incidence of Sciaridae larvae. In axenic cultivation, it may occur only after the casing layer phase. Therefore if A. brasiliensis, in axenic cultivation, efficiently convert substrate with low C:N ratio (high N content) into basidiocarps, the use of this method for commercial purposes may become economically viable.

It was observed that the mycelial growth showed two distinct types of mycelia according to the level of mycelial density (Table 2). For C:N ratios from 11:1 to 50:1 (N from 4.25 to 0.98%), the mycelial growth was denser and similar to the one obtained in the MEA culture media (C:N = 17:1; N 2.90%; Table 2). For C:N ratios from 100:1 to 248:1 (N from 0.50 to 0.20%), the mycelium presented more disperse ramification (Table 2), which is typical in substrate with nutritional limitation, according to Carlile and Watkinson (1995). Comparing the mycelial growth in the substrate with C:N ratio of 100:1 to C:N ratio of 50:1, they were found equal (p < 0.05; Figure 1). However a more disperse mycelial ramification on C:N ration of 100:1 because of nutritional limitation to the mycelial growth showed the opposite (Table 2). The negative control (C:N = 500:1, estimated), with agar only, showed a mycelial growth with very disperse ramifications which indicates a complete draining of nutrients that were provided by the cylinder with MEA culture media (Table 2).

Conclusion

Substrate with soybean fiber alone provide higher mycelial growth than any mixture with cassava fiber; the highest mycelial growth on substrate is with C:N ratio of 11:1 (N = 4.25%); the intermediate growth is with C:N ratio range from 15:1 to 50:1 (N from 3.31% to 0.98%); and the lower growth is with C:N ratio of 100:1 or higher (N < 0.50%).

Acknowledgements

We thank UNIPAR/DEGES/Coordmation of the Biology Sciences Course - Biotechnology, UNIPAR/DEGPP/COPIC, Fundação Araucária and CNPq for financial support.

References

ANDRADE, M. C. N.; KOPYTOWSKI FILHO, J.; MINHONI, M. T. A.; COUTINHO, L. N.; FIGUEIREDO, M. B. Productivity, biological efficiency, and number of Agaricus blazei mushrooms grown in compost in the presence of Trichoderma sp. and Chaetomium olivacearum contaminants. Brazilian Journal of Microbiology, v. 38, n. 2, p. 243-247, 2007.

BRAGA, G. C.; EIRA, A. F.; CELSO, P. G.; COLAUTO, N. B. Manual do cultivo de Agaricus blazei Murr. 'Cogumelo-do-Sol'. Botucatu: Fepaf, 1998.

CARLILE, M. J.; WATKINSON, S. C. The fungi. 2^nd ed. San Diego: Academic, 1995.

CHANG, S. T.; MILES, P. G. Edible mushrooms and their cultivation. Boca Raton: CRC, 1989.

COLAUTO, N. B.; DIAS, E. S.; GIMENES, M. A.; EIRA, A. F. Genetic characterization of isolates of the basidiomycete Agaricus blazei by RAPD. Brazilian Journal of Microbiology, v. 33, n. 2, p. 131-133, 2002.

DIAS, E. S.; ABE, C.; SCHWAN, R. F. Truths and myths about the mushroom Agaricus blazei. Scientia Agricola, v. 61, n. 5, p. 545-549, 2004.

DONINI, L. P.; BERNARDI, E.; NASCIMENTO, J. S. Desenvolvimento in vitro de Agaricus brasiliensis em meios suplementados com diferentes farelos. Pesquisa Agropecuária Brasileira, v. 41, n. 6, p. 995-999, 2006.

EIRA, A. F. Cultivo do cogumelo medicinal -Agaricus blazei (Murril) ss. Heinemann ou Agaricus brasiliensis (Wasser et al.). Viçosa: Aprenda Fácil, 2003.

EIRA, A. F.; NASCIMENTO, J. S.; COLAUTO, N. B.; CELSO, P. G. Tecnologia de cultivo do cogumelo medicinal Agaricus blazei (Agaricus brasiliensis). Agropecuária Catarinense, v. 18, n. 3, p. 45-49, 2005.

GERRITS, J. P. G. Nutrition and compost. In: VAN GRIENSVEN, L. J. L. D. (Ed.). The cultivation of mushrooms. Horst: Mushroom Experimental Station, 1988. p. 29-38.

HERNANDEZ, D.; SANCHEZ, J. E.; YAMASAKI, K. A simple procedure for preparing substrate for Pleurotus ostreatus cultivation. Bioresource Tecnology, v. 90, n. 2, p. 145-150, 2003.

HSIEH, C.; YANG, F. C. Reusing soy residue for the solid-state fermentation of Ganoderma lucidum. Bioresource Tecnology, v. 91, n. 1, p. 105-109, 2004.

IBGE-Instituto Brasileiro de Geografia e Estatística. Levantamento sistemático da produção agrícola de 2006. Disponível em: <http://www.ibge.gov.br/ome/estatistica/indicadores/agropecuaria/lspa/lspa_200707_5.shtm>. Acesso em: 6 set. 2007.

KAMRA, D. N.; ZADRAZIL, F. Influence of gaseous phase, light and substrate pretreatment on fruit-body formation, lignin degradation and in vitro digestibility of wheat straw fermented with Pleurotus spp. Agricultural Wastes, v. 18, n. 1, p. 1-17, 1986.

KERRIGAN, R. W. Agaricus subrufescens, a cultivated edible and medicinal mushroom, and its synonyms. Mycologia, v. 97, n. 1, p. 12-24, 2005.

KIM, Y. W.; KIM, K. H.; CHOI, H. J.; LEE, D. S. Antidiabetic activity of β-glucans and their enzymatically hydrolyzed oligosaccharides from Agaricus blazei. Biotechnology Letters, v. 27, n. 7, p. 483-487, 2005.

KIMURA, Y.; KIDO, T.; TAKAKU, T.; SUMIYOSHI, M.; BABA, K. Isolation of an anti-angiogenic substance from Agaricus blazei Murill: its antitumor and antimetastatic actions. Cancer Science, v. 95, n. 9, p. 758-764, 2004.

KOPYTOWSKI FILHO, J.; MINHONI, M. T. A. Calorific value and carbon content of Agaricus blazei Murrill compost in relationship to C/N ratio and protein sources proportion. Energia na Agricultura, v. 18, n. 2, p. 34-40, 2003.

LARA, A. B. W. H.; NAZÁRIO, G.; ALMEIDA, M. E. W.; PREGNOLATTO, W. Normas analíticas do Instituto Adolfo Lutz: métodos químicos e físicos para análise de alimentos. São Paulo: Instituto Adolfo Lutz, 1976.

LEONEL, M.; CEREDA, M. P.; ROAU, X. Aproveitamento do resíduo da produção de etanol a partir de farelo de mandioca, como fonte de fibras dietéticas. Ciência e Tecnologia de Alimentos, v. 19, n. 2, p. 241-245, 1999.

LINDE, G. A.; MACHADO, R. P. Fibra de soja: benefícios à saúde e aplicações. Food Ingredients, v. 11, n. 3, p. 28-32, 2001.

MACAYA-LIZANO, A. V. Cultivo de Pleurotus ostreatus y especies afines (Fungi: Pleurotaceae) sobre medios naturales semi-estériles. Revista de Biologia Tropical, v. 36, n. 2a, p. 255-260, 1988.

MACCANNA, C. Commercial mushroom production. Dublin: Kinsealy Research Centre, 1984.

MANTOVANI, T. R. D.; LINDE, G. A.; COLAUTO, N. B. Effect of the addition of nitrogen sources to cassava fiber and carbon-to-nitrogen ratios on Agaricus brasiliensis growth. Canadian Journal of Microbiology, v. 53, n. 1, p. 139-143, 2007.

MENZEL, F.; SMITH, J. E.; COLAUTO, N. B. Bradysia difformis Frey and Bradysia ocellaris (Comstock): two additional neotropical species of Black Fungus Gnats (Diptera: Sciaridae) of economic importance: a redescription and review. Annals of the Entomological Society of America, v. 96, n. 4, p. 448-457, 2003.

MILES, P. G.; CHANG, S. T. Mushroom biology: concise basics and current developments. Singapore: World Scientific, 1997.

MIZUNO, T. Medicinal properties and clinical effects of culinary-medicinal mushroom Agaricus blazei Murrill (Agaricomycetideae). International Journal of Medicinal Mushrooms, v. 4, n. 4, p. 299-312, 2002.

OEI, P. Mushroom cultivation. Leiden: Tool, 1996.

OSHIMAN, K.; FUJIMIYA, Y.; EBINA, T.; SUZUKI, I.; NOJI, M. Orally administered beta-1,6-D-polyglucose extracted from Agaricus blazei results in tumor regression in tumor-bearing mice. Planta Medica, v. 68, n. 7, p. 610-614, 2002.

RAJARATHNAM, S.; BANO, Z. Pleurotus mushrooms: part III. Biotransformations of natural lignocellulosic wastes: commercial applications and implications. Critical Reviews in Food Science and Nutrition, v. 28, n. 1, p. 31-113, 1989.

RODRIGUES, S. B.; JABOR, I. A. S.; MARQUES-SILVA, G. G.; ROCHA, C. L. M. S. C. Avaliação do potencial antimutagênico do cogumelo do sol (Agaricus blazei) no sistema methG1 em Aspergillus (=Emericella). Acta Scientiarum. Agronomy, v. 25, n. 2, p. 513-517, 2003.

ROSSI, I. H.; MONTEIRO, A. C.; MACHADO, J. O.; BARBOSA, J. C. Supplementation of sugarcane bagasse with rice bran and sugarcane molasses for shiitake (Lentinula edodes) spawn production. Brazilian Journal of Microbiology, v. 34, n. 1, p. 61-65, 2003.

SANCHEZ, C. Modern aspects of mushroom culture technology. Applied Microbiology and Biotechnology, v. 64, n. 6, p. 756-762, 2004.

SOUZA-PACCOLA, E. A.; BOMFETI, C. A.; FÁVARO, L. C. L.; FONSECA, I. C. B.; PACCOLA-MEIRELLES, L. D. Antimutagenic action of Lentinula edodes and Agaricus blazei on Aspergillus nidulans conidia. Brazilian Journal of Microbiology, v. 35, n. 4, p. 311-315, 2004.

SRIVASTAVA, H. C.; BANO, Z. Nutrition requirements of Pleurotus fabellatus. Applied and Environmental Microbiology, v. 19, n. 1, p. 166-169, 1970.

STRAATSMA, G.; GERRITS, J. P. G.; THISSEN, J. T. N. M.; AMSING, J. G. M.; LOEFFEN, H.; VAN GRIENSVEN, L. J. L. D. Adjustment of the composting process for mushroom cultivation based on initial substrate composition. Bioresource Technology, v. 72, n. 1, p. 67-74, 2000.

VAN GRIENSVEN, L. J. L. D. The cultivation of mushrooms. Horst: Mushroom Experimental Station, 1988. WASSER, S. P.; DIDUKH, M. Y.; AMAZONAS, M. A. L. A.; NEVO, E.; STAMETS, P.; EIRA, A. F. Is a widely cultivated culinary-medicinal royal sun Agaricus (the himematsutake mushroom) indeed Agaricus blazei Murrill? International Journal of Medicinal Mushrooms, v. 4, n. 4, p. 267-290, 2002.

WU, J. Z.; CHEUNG, P. C. K.; WONG, K. H.; HUANG, N. I. Studies on submerged fermentation of Pleurotus tuber-regium (Fr.) Singer. Part 2: effect of carbon-to-nitrogen ratio of culture medium on the content and composition of the mycelial dietary fibre. Food Chemistry, v. 85, n. 1, p. 101-105, 2004.

ZADRAZIL, F. Influence of ammonium nitrate and organic supplements on the yield of Pleurotus sajor-caju (Fr.) Sing. Applied Microbiology and Biotechnology, v. 9, n. 1, p. 31-35, 1980.

ZHEN, F. Q.; YANG, R. C.; LIU, R. X.; ZHEN, F. Q.; YANG, R. C.; LIU, R. X. Effects of different C:N ratios in compost on nutrient transformation and on yield and quality of Agaricus bisporus. Acta Agriculturae Shanghai, v. 11, n. 1, p. 33-38, 1995.

Received on September 16, 2008.

Accepted on March 3, 2009.

License information: This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

References

• ANDRADE, M. C. N.; KOPYTOWSKI FILHO, J.; MINHONI, M. T. A.; COUTINHO, L. N.; FIGUEIREDO, M. B. Productivity, biological efficiency, and number of Agaricus blazei mushrooms grown in compost in the presence of Trichoderma sp. and Chaetomium olivacearum contaminants. Brazilian Journal of Microbiology, v. 38, n. 2, p. 243-247, 2007.
• BRAGA, G. C.; EIRA, A. F.; CELSO, P. G.; COLAUTO, N. B. Manual do cultivo de Agaricus blazei Murr. 'Cogumelo-do-Sol'. Botucatu: Fepaf, 1998.
• CARLILE, M. J.; WATKINSON, S. C. The fungi. 2^nd ed. San Diego: Academic, 1995.
• CHANG, S. T.; MILES, P. G. Edible mushrooms and their cultivation. Boca Raton: CRC, 1989.
• COLAUTO, N. B.; DIAS, E. S.; GIMENES, M. A.; EIRA, A. F. Genetic characterization of isolates of the basidiomycete Agaricus blazei by RAPD. Brazilian Journal of Microbiology, v. 33, n. 2, p. 131-133, 2002.
• DIAS, E. S.; ABE, C.; SCHWAN, R. F. Truths and myths about the mushroom Agaricus blazei. Scientia Agricola, v. 61, n. 5, p. 545-549, 2004.
• DONINI, L. P.; BERNARDI, E.; NASCIMENTO, J. S. Desenvolvimento in vitro de Agaricus brasiliensis em meios suplementados com diferentes farelos. Pesquisa Agropecuária Brasileira, v. 41, n. 6, p. 995-999, 2006.
• EIRA, A. F. Cultivo do cogumelo medicinal -Agaricus blazei (Murril) ss. Heinemann ou Agaricus brasiliensis (Wasser et al.). Viçosa: Aprenda Fácil, 2003.
• EIRA, A. F.; NASCIMENTO, J. S.; COLAUTO, N. B.; CELSO, P. G. Tecnologia de cultivo do cogumelo medicinal Agaricus blazei (Agaricus brasiliensis). Agropecuária Catarinense, v. 18, n. 3, p. 45-49, 2005.
• GERRITS, J. P. G. Nutrition and compost. In: VAN GRIENSVEN, L. J. L. D. (Ed.). The cultivation of mushrooms. Horst: Mushroom Experimental Station, 1988. p. 29-38.
• HERNANDEZ, D.; SANCHEZ, J. E.; YAMASAKI, K. A simple procedure for preparing substrate for Pleurotus ostreatus cultivation. Bioresource Tecnology, v. 90, n. 2, p. 145-150, 2003.
• HSIEH, C.; YANG, F. C. Reusing soy residue for the solid-state fermentation of Ganoderma lucidum. Bioresource Tecnology, v. 91, n. 1, p. 105-109, 2004.
• IBGE-Instituto Brasileiro de Geografia e Estatística. Levantamento sistemático da produção agrícola de 2006 Disponível em: <http://www.ibge.gov.br/ome/estatistica/indicadores/agropecuaria/lspa/lspa_200707_5.shtm>. Acesso em: 6 set. 2007.
• KAMRA, D. N.; ZADRAZIL, F. Influence of gaseous phase, light and substrate pretreatment on fruit-body formation, lignin degradation and in vitro digestibility of wheat straw fermented with Pleurotus spp. Agricultural Wastes, v. 18, n. 1, p. 1-17, 1986.
• KERRIGAN, R. W. Agaricus subrufescens, a cultivated edible and medicinal mushroom, and its synonyms. Mycologia, v. 97, n. 1, p. 12-24, 2005.
• KIM, Y. W.; KIM, K. H.; CHOI, H. J.; LEE, D. S. Antidiabetic activity of β-glucans and their enzymatically hydrolyzed oligosaccharides from Agaricus blazei. Biotechnology Letters, v. 27, n. 7, p. 483-487, 2005.
• KIMURA, Y.; KIDO, T.; TAKAKU, T.; SUMIYOSHI, M.; BABA, K. Isolation of an anti-angiogenic substance from Agaricus blazei Murill: its antitumor and antimetastatic actions. Cancer Science, v. 95, n. 9, p. 758-764, 2004.
• KOPYTOWSKI FILHO, J.; MINHONI, M. T. A. Calorific value and carbon content of Agaricus blazei Murrill compost in relationship to C/N ratio and protein sources proportion. Energia na Agricultura, v. 18, n. 2, p. 34-40, 2003.
• LARA, A. B. W. H.; NAZÁRIO, G.; ALMEIDA, M. E. W.; PREGNOLATTO, W. Normas analíticas do Instituto Adolfo Lutz: métodos químicos e físicos para análise de alimentos. São Paulo: Instituto Adolfo Lutz, 1976.
• LEONEL, M.; CEREDA, M. P.; ROAU, X. Aproveitamento do resíduo da produção de etanol a partir de farelo de mandioca, como fonte de fibras dietéticas. Ciência e Tecnologia de Alimentos, v. 19, n. 2, p. 241-245, 1999.
• LINDE, G. A.; MACHADO, R. P. Fibra de soja: benefícios à saúde e aplicações. Food Ingredients, v. 11, n. 3, p. 28-32, 2001.
• MACAYA-LIZANO, A. V. Cultivo de Pleurotus ostreatus y especies afines (Fungi: Pleurotaceae) sobre medios naturales semi-estériles. Revista de Biologia Tropical, v. 36, n. 2a, p. 255-260, 1988.
• MACCANNA, C. Commercial mushroom production. Dublin: Kinsealy Research Centre, 1984.
• MANTOVANI, T. R. D.; LINDE, G. A.; COLAUTO, N. B. Effect of the addition of nitrogen sources to cassava fiber and carbon-to-nitrogen ratios on Agaricus brasiliensis growth. Canadian Journal of Microbiology, v. 53, n. 1, p. 139-143, 2007.
• MENZEL, F.; SMITH, J. E.; COLAUTO, N. B. Bradysia difformis Frey and Bradysia ocellaris (Comstock): two additional neotropical species of Black Fungus Gnats (Diptera: Sciaridae) of economic importance: a redescription and review. Annals of the Entomological Society of America, v. 96, n. 4, p. 448-457, 2003.
• MILES, P. G.; CHANG, S. T. Mushroom biology: concise basics and current developments. Singapore: World Scientific, 1997.
• MIZUNO, T. Medicinal properties and clinical effects of culinary-medicinal mushroom Agaricus blazei Murrill (Agaricomycetideae). International Journal of Medicinal Mushrooms, v. 4, n. 4, p. 299-312, 2002.
• OEI, P. Mushroom cultivation. Leiden: Tool, 1996.
• OSHIMAN, K.; FUJIMIYA, Y.; EBINA, T.; SUZUKI, I.; NOJI, M. Orally administered beta-1,6-D-polyglucose extracted from Agaricus blazei results in tumor regression in tumor-bearing mice. Planta Medica, v. 68, n. 7, p. 610-614, 2002.
• RAJARATHNAM, S.; BANO, Z. Pleurotus mushrooms: part III. Biotransformations of natural lignocellulosic wastes: commercial applications and implications. Critical Reviews in Food Science and Nutrition, v. 28, n. 1, p. 31-113, 1989.
• RODRIGUES, S. B.; JABOR, I. A. S.; MARQUES-SILVA, G. G.; ROCHA, C. L. M. S. C. Avaliação do potencial antimutagênico do cogumelo do sol (Agaricus blazei) no sistema methG1 em Aspergillus (=Emericella). Acta Scientiarum. Agronomy, v. 25, n. 2, p. 513-517, 2003.
• ROSSI, I. H.; MONTEIRO, A. C.; MACHADO, J. O.; BARBOSA, J. C. Supplementation of sugarcane bagasse with rice bran and sugarcane molasses for shiitake (Lentinula edodes) spawn production. Brazilian Journal of Microbiology, v. 34, n. 1, p. 61-65, 2003.
• SANCHEZ, C. Modern aspects of mushroom culture technology. Applied Microbiology and Biotechnology, v. 64, n. 6, p. 756-762, 2004.
• SOUZA-PACCOLA, E. A.; BOMFETI, C. A.; FÁVARO, L. C. L.; FONSECA, I. C. B.; PACCOLA-MEIRELLES, L. D. Antimutagenic action of Lentinula edodes and Agaricus blazei on Aspergillus nidulans conidia. Brazilian Journal of Microbiology, v. 35, n. 4, p. 311-315, 2004.
• SRIVASTAVA, H. C.; BANO, Z. Nutrition requirements of Pleurotus fabellatus. Applied and Environmental Microbiology, v. 19, n. 1, p. 166-169, 1970.
• STRAATSMA, G.; GERRITS, J. P. G.; THISSEN, J. T. N. M.; AMSING, J. G. M.; LOEFFEN, H.; VAN GRIENSVEN, L. J. L. D. Adjustment of the composting process for mushroom cultivation based on initial substrate composition. Bioresource Technology, v. 72, n. 1, p. 67-74, 2000.
• VAN GRIENSVEN, L. J. L. D. The cultivation of mushrooms. Horst: Mushroom Experimental Station, 1988.
• WASSER, S. P.; DIDUKH, M. Y.; AMAZONAS, M. A. L. A.; NEVO, E.; STAMETS, P.; EIRA, A. F. Is a widely cultivated culinary-medicinal royal sun Agaricus (the himematsutake mushroom) indeed Agaricus blazei Murrill? International Journal of Medicinal Mushrooms, v. 4, n. 4, p. 267-290, 2002.
• WU, J. Z.; CHEUNG, P. C. K.; WONG, K. H.; HUANG, N. I. Studies on submerged fermentation of Pleurotus tuber-regium (Fr.) Singer. Part 2: effect of carbon-to-nitrogen ratio of culture medium on the content and composition of the mycelial dietary fibre. Food Chemistry, v. 85, n. 1, p. 101-105, 2004.
• ZADRAZIL, F. Influence of ammonium nitrate and organic supplements on the yield of Pleurotus sajor-caju (Fr.) Sing. Applied Microbiology and Biotechnology, v. 9, n. 1, p. 31-35, 1980.
• ZHEN, F. Q.; YANG, R. C.; LIU, R. X.; ZHEN, F. Q.; YANG, R. C.; LIU, R. X. Effects of different C:N ratios in compost on nutrient transformation and on yield and quality of Agaricus bisporus. Acta Agriculturae Shanghai, v. 11, n. 1, p. 33-38, 1995.

Publication Dates

• Publication in this collection
  24 Nov 2011
• Date of issue
  Mar 2010

History

• Received
  16 Sept 2008
• Accepted
  03 Mar 2009