Abstract
Spent mushroom substrate (SMS) of Pleurotus ostreatus was supplemented with wheat bran and soybean flour in various proportions to obtain C/N ratios of 10, 20, and 30, and their effect was evaluated in successive cultivation of Pleurotus ostreatus, Pleurotus pulmonarius, Ganoderma adspersum, Ganoderma resinaceum, and Lentinula edodes strains with respect to mycelium growth rate, biomass concentration, recovery of the enzyme laccase and crude exopolysaccharides, and also with additional fruiting body production. All fungi showed the highest growth rate on unamended SMS (C/N 30), with G. resinaceum being the fastest colonizer (Kr = 9.84 mm day−1), while biomass concentration maximized at C/N 10. Moreover, supplementation affected positively laccase activity, with P. pulmonarius furnishing the highest value (44,363.22 U g−1) at C/N 20. On the contrary, L. edodes growth, fruiting, and laccase secretion were not favored by SMS supplementation. Fruiting body formation was promoted at C/N 30 for Ganoderma and at C/N 20 for Pleurotus species. Exopolysaccharide production of further studied Pleurotus strains was favored at a C/N 20 ratio, at the initial stage of SMS colonization. The obtained results support the potential effective utilization of supplemented SMS for laccase production from Ganoderma spp. and for new fruiting body production of Pleurotus spp.




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Ahlawat OP, Sagar MP (2007) Management of spent mushroom substrate, National Research Centre for Mushroom, Solan (ed) Indian Council of Agricultural Research, Chambaghat, Solan, India
APHA AWWA and WPCF (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, American Water Works Association, Water Environment Federation, Washington, DC, USA
Ashrafi R, Mian MH, Rahman MM, Jahiruddin M (2014) Recycling of spent mushroom substrate for the production of oyster mushroom. Res Biotechnol 5:13–21
Badham ER (1989) Influence of water potential on growth of shiitake mycelium. Mycologia 81:464–468
Berovic M, Svagelj M, Habijanic J, Gregori A, Boh B, Pankl M, Wraber B (2015) Cultivation of the medicinal mushroom Ganoderma lucidum and Grifola frondosa mycelia and polysaccharides in bioreactors. Proceedings of the 3rd international conference on advances in applied science and environmental engineering-ASEE, Institute of research engineers and doctors, New York, USA
Buendia RP, Rardo-Gimenez A, de Juan-Valero JA (2016) Reuse of degraded Pleurotus ostreatus (jacq.) P. Kumm. substrate by supplementation with wheat bran. Quantitative parameters. Mycology 7:1–11
Chang ST, Miles PG (2004) Mushrooms: cultivation, nutritional value, medicinal effect and environmental impact, 2nd edn. CRC Press, Boca Raton, Florida, USA
Chen GQ, Zeng GM, Tu X, Huang GH, Chen YN (2005) A novel biosorbent: characterization of the spent mushroom compost and its application for removal of heavy metals. J Environ Sci 17:756–760
Cheung PC (2008) Mushrooms as functional food. Wiley, New York, USA
D Agostini ÉC, Rafaele T, Mantovani DA, Silveira J, Paccola-meirelles D, Colauto NB, Linde GA (2011) Low carbon/nitrogen ratio increases laccase production from basidiomycetes in solid substrate cultivation. Sci Agr 68(3):295–300
Diamantopoulou P, Papanikolaou S, Katsarou E, Komaitis M, Aggelis G, Philippoussis A (2012) Mushroom polysaccharides and lipids synthesized in liquid agitated and static cultures. Part II: study of Volvariella volvacea. Appl Biochem Biotech 167:1890–1906
Diamantopoulou P, Papanikolaou S, Komaitis M, Aggelis G, Philippoussis A (2014) Patterns of major metabolites biosynthesis by different mushroom fungi grown on glucose-based submerged cultures. Bioprocess Biosyst Eng 37:1385–1400
Diamantopoulou P, Philippoussis A (2015) Cultivated mushrooms: preservation and processing. In: Hui YH (ed) Handbook of vegetable preservation and processing. CRC press, Florida, pp 495–525
Elisashvili V, Kachlishvili E, Asatiani MD (2015) Shiitake medicinal mushroom, Lentinus edodes (higher basidiomycetes) productivity and lignocellulolytic enzyme profiles during wheat straw and tree leaf bioconversion. Int J Med Mushrooms 17:77–86
Juárez RAC, Dorry LLG, Bello-Mendoza R, Sánchez JE (2011) Use of spent substrate after Pleurotus pulmonarius cultivation for the treatment of chlorothalonil containing wastewater. J Environ Manage 92(3):948–952
Hirasawa M, Shouji N, Neta T, Fukushima K, Takada K (1999) Three kinds of antibacterial substances from Lentinus edodes (Berk.) sing. (shiitake, an edible mushroom). Int J Antimicrob Agents 11:151–157
Hublik G, Schinner F (2000) Characterization and immobilization of the laccase from Pleurotus ostreatus and its use for the continuous elimination of phenolic pollutants. Enzyme Microb Tech 27:330–336
Israilides C, Kletsas D, Arapoglou D, Philippoussis A, Pratsinis H, Ebringerova A, Hribalova V, Harding SE (2008) In vitro cytostatic and immunomodulatory properties of the medicinal mushroom Lentinula edodes. Phytomedicine 15:512–519
Kachlishvili E, Penninckx MJ, Tsiklauri N, Elisashvili V (2006) Effect of nitrogen source on lignocellulolytic enzyme production by white-rot basidiomycetes under solid-state cultivation. World J Microbiol Biotechnol 22:391–397
Kao PF, Wang SH, Hung WT, Liao YH, Lin CM, Yang WB (2012) Structural characterization and antioxidative activity of low-molecular-weights β-1,3-glucan from the residue of extracted Ganoderma lucidum fruiting bodies. J Biomed Biotechnol 2012:1–8
Ko HG, Park SH, Kim SH, Park HG, Park WM (2005) Detection and recovery of hydrolytic enzymes from spent compost of four mushroom species. Folia Microbiol 50:103–106
Koutrotsios G, Mountzouris KC, Chatzipavlidis I, Zervakis GI (2014) Bioconversion of lignocellulosic residues by Agrocybe cylindracea and Pleurotus ostreatus mushroom fungi—assessment of their effect on the final product and spent substrate properties. Food Chem 161:127–135
Kozarski M, Klaus A, Niksic M, Jakovljevic D, Helsper JPFG, Van Griensven LJLD (2011) Antioxidative and immunomodulating activities of polysaccharide extracts of the medicinal mushrooms Agaricus bisporus, Agaricus brasiliensis, Ganoderma lucidum and Phellinus linteus. Food Chem 129:1667–1675
Kurt S, Buyukalaca S (2010) Yield performances and changes in enzyme activities of Pleurotus spp. (P. ostreatus and P. sajor-caju) cultivated on different agricultural wastes. Bioresour Technol 101:3164–3169
Lau KL, Tsang YY, Chiu SW (2003) Use of spent mushroom compost to bioremediate PAH-contaminated samples. Chemosphere 52:1539–1546
Mandeel QA, Al-Laith AA, Mohamed SA (2005) Cultivation of oyster mushrooms (Pleurotus spp.) on various lignocellulosic wastes. World J Microbiol Biotechnol 21:601–607
Matute RG, Figlas D, Curvetto N (2011) Agaricus blazei production on non-composted substrates based on sunflower seed hulls and spent oyster mushroom substrate. World J Microbiol Biotechnol 27:1331–1339
Osińska-Jaroszuk M, Jaszek M, Mizerska-Dudka M, Błachowicz A, Rejczak TP, Janusz G, Wydrych J, Polak J, Jarosz-WilkoBazka A, Kandefer-Szerszeń M (2014) Exopolysaccharide from Ganoderma applanatum as a promising bioactive compound with cytostatic and antibacterial properties. Biomed Res Int 2014:1–10
Phan CW, Sabaratnam V (2012) Potential uses of spent mushroom substrate and its associated lignocellulosic enzymes. Appl Microbiol Biotechnol 96:863–873
Philippoussis A (2009) Production of mushrooms using agro-industrial residues as substrates. In: Sing Nigam P, Pandey A (eds) Biotechnology for agro-industrial residues processing. Springer, Berlin, pp 163–196
Philippoussis A, Diamantopoulou P (2012) Exploitation of the biotechnological potential of agro-industrial by-products through mushroom cultivation. In: Petre M, Berovic M (eds) Mushroom biotechnology and bioengineering. University of Pitesti, Bucharest, pp 161–184
Philippoussis A, Zervakis G, Diamantopoulou P (2001) Bioconversion of lignocellulosic wastes through the cultivation of the edible mushrooms Agrocybe aegerita, Volvariella volvacea and Pleurotus spp. World J Microbiol Biotechnol 17:191–200
Philippoussis A, Diamantopoulou P, Zervakis G (2003) Correlation of the properties of several lignocellulosic substrates to the crop performance of the shiitake mushroom Lentinula edodes. World J Microbiol Biotechnol 19:551–557
Philippoussis A, Diamantopoulou P, Israilides C (2007) Productivity of agricultural residues used for the cultivation of the medicinal fungus Lentinula edodes. Int Biodeterior Biodegradation 59:216–219
Philippoussis A, Diamantopoulou P, Papadopoulou K, Lakhtar H, Roussos S, Parissopoulos G, Papanikolaou S (2011) Biomass, laccase and endoglucanase production by Lentinula edodes during solid state fermentation of reed grass, bean stalks and wheat straw residues. World J Microbiol Biotechnol 27:285–297
Rigas F, Papadopoulou K, Philippoussis A, Papadopoulou M, Chatzipavlidis J (2009) Bioremediation of lindane contaminated soil by Pleurotus ostreatus in non sterile conditions using multilevel factorial design. Water Air Soil Poll 197:121–129
Royse DJ (1992) Recycling of spent shiitake substrate for production of the oyster mushroom, Pleurotus sajor-caju. Appl Microbiol Biotechnol 38:179–182
Shashirekha MN, Rajarathnam S, Bano Z (2002) Enhancement of bioconversion efficiency and chemistry of the mushroom, Pleurotus sajor-caju (Berk and Br.) Sacc. produced on spent rice straw substrate, supplemented with oil seed cakes. Food Chem 76:27–31
Singh AD, Abdullah N, Vikineswary S (2003) Optimization of extraction of bulk enzymes from spent mushroom compost. J Chem Technol Biot 78:743–752
Singh AD, Sabaratnam V, Abdullah N, Annuar MSM, Ramachandran KB (2010) Decolourisation of chemically different dyes by enzymes from spent compost of Pleurotus sajor-caju and their kinetics. Afr J Biotechnol 9:41–54
Smiderle FR, Olsen LM, Ruthes AC, Czelusniak PA, Santana-Filho AP, Sassaki PAJ, Iacomini GM (2012) Exopolysaccharides, proteins and lipids in Pleurotus pulmonarius submerged culture using different carbon sources. Carbohyd Polym 87:368–376
Songulashvili G, Elisashvili V, Wasser PS, Nevo E, Hadar Y (2007) Basidiomycetes laccase and manganese peroxidase activity in submerged fermentation of food industry wastes in submerged fermentation of food industry wastes. Enzyme Microb Tech 41:57–61
Svagelj M, Berovic M, Boh B, Menard A, Simcic S, Wraber B (2008) Solid-state cultivation of Grifola frondosa (dicks: Fr) S.F. Gray biomass and immunostimulatory effects of fungal intra- and extracellular beta-polysaccharides. New Biotechnol 25:150–156
Telles CBS, Sabry DA, Almeida-Lima J, Costa MSSP, Melo-Silveira RF, Trindade ES, Sassaki GL, Wisbeck E, Furlan SA, Leite EL, Rocha HAO (2011) Sulfation of the extracellular polysaccharide produced by the edible mushroom Pleurotus sajor-caju alters its antioxidant, anticoagulant and antiproliferative properties in vitro. Carbohyd Polym 85:514–521
Thompson WH (2001) Test methods for the examination of composting and compost. The United States composting council research and education foundation. The United States Department of Agriculture, Washington, DC
Trejo-Hernandez MR, Lopez-Munguia A, Quintero Ramirez R (2001) Residual compost of Agaricus bisporus as a source of crude laccase for enzymic oxidation of phenolic compounds. Process Biochem 36:635–639
Wang S, Xu F, Li Z, Zhao S, Song S, Rong C, Geng X, Liu Y (2015) The spent mushroom substrates of Hypsizigus marmoreus can be an effective component for growing the oyster mushroom Pleurotus ostreatus. Sci Hort 186:217–222
Wasser SP (2002) Medicinal mushroom as a source of antitumor and immunomodulating polysaccharides. Appl Microbiol Biotechnol 60:258–274
Wasser SP (2010a) Reishi. In: Coates PM, Betz JM, Blackman MR, Cragg GM, Levine M, Mass J, White JD (ed) Encyclopedia of dietary supplements, 2nd (eds) Informa Healthcare, New York and London, pp 680–690
Wasser SP (2010b) Shiitake. In: Coates PM, Betz JM, Blackman MR, Cragg GM, Moss MLJ (eds) Encyclopedia of dietary supplements, 2nd edn. Informa Healthcare, New York and London, pp 719–726
Wasser SP (2014) Medicinal mushroom science: current perspectives, advances, evidences and challenges. Biom J 37:345–356
Yuan B, Zhang W, Yu Z, Zhang R (2012) In vitro evaluation of antioxidant property of the exopolysaccharides peptides from Ganoderma lucidum CAU5501 in submerged culture. J Food Agric Environ 10:97–101
Zhu H, Sheng K, Yan E, Qiao J, Lv F (2012) Extraction, purification and antibacterial activities of a polysaccharide from spent mushroom substrate. Int J Biol Macromol 50:840–843
Acknowledgements
This work was supported by the Project “Research & Technology Development Innovation Projects”—AgroETAK, MIS 453350, in the framework of the Operational Program “Human Resources Development.” It was co-funded by the European Social Fund through the National Strategic Reference Framework (Research Funding Program 2007–2013) coordinated by the Hellenic Agricultural Organization—DEMETER (Institute of Technology of Agricultural Products/Laboratory of Edible Fungi).
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Economou, C.N., Diamantopoulou, P.A. & Philippoussis, A.N. Valorization of spent oyster mushroom substrate and laccase recovery through successive solid state cultivation of Pleurotus, Ganoderma, and Lentinula strains. Appl Microbiol Biotechnol 101, 5213–5222 (2017). https://doi.org/10.1007/s00253-017-8251-3
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DOI: https://doi.org/10.1007/s00253-017-8251-3


