Skip to main content
SpringerLink
Log in

Biomass, laccase and endoglucanase production by Lentinula edodes during solid state fermentation of reed grass, bean stalks and wheat straw residues

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Mycelium growth rates, biomass concentration (estimated as glucosamine content) and laccase and endoglucanase secretion were monitored during solid state fermentation (SSF) of wheat straw (WS), reed grass (RG) and bean stalk (BS) residues by Lentinula edodes strains 119, 121, and 122. In a first experiment, these strains were subjected to screening regarding their growth rates and biomass yield, where strain 121 proved to be the fastest colonizer. However, the greater biomass yield at the end of colonization was demonstrated by strain 122 on BS (465.93 mg g−1 d.w.). In a second experiment, growth characters, as well as endoglucanase and laccase production patterns of the selected strains 121 and 122 were monitored at three intervals i.e., at 33, 66, and 100% of substrate colonization. BS furnished the highest endoglucanase production for strain 121, while RG for strain 122. A strain and substrate-dependent behaviour of the enzyme secretion was detected, with strain 122 presenting maximal endoglucanase activity in all substrates at the initial (33%) and final (100%) stages of colonization (0.64–0.90 and 0.79–0.97 U g−1, respectively). However, in strain 121 the peak of endoglucanase production was detected in the early stages of colonization (at 33% on WS and at 66% on RG and BS). Laccase activity showed increased values (maxima on WS, 353.68 and 548.67 U g−1 by strains 121 and 122, respectively) at 66% of colonization. Correlation analysis of growth data demonstrated negative relations between growth rate and biomass yield and between laccase and endoglucanase activities on WS and RG substrates fermented by strain 122. Finally, possible relations of growth parameters with nutritional constituents of the substrates were investigated.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Albrecht R, Ziarelli F, Alarcón-Gutiérrez E, Petit JL, Terrom G, Perissol C (2008) 13C solid-state NMR assessment of decomposition pattern during co-composting of sewage sludge and green wastes. Eur J Soil Sci 59(3):445–452

    Article  Google Scholar 

  • Arai Y, Shirasaka N, Yoshikawa K, Kitamoto Y, Suzuki A, Sakamoto R, Sata H, Terashita T (2005) The stimulation of extracellular carbohydrases of edible mushrooms by the hot water-soluble fraction from corn fiber. Mycoscience 46:235–240

    Article  CAS  Google Scholar 

  • Bhat MK (2000) Cellulases and related enzymes in biotechnology. Biotechnol Adv 18:355–383

    Article  CAS  Google Scholar 

  • Bollag JM, Shuttleworth LK, Anderson HD (1988) Laccase mediated detoxification of phenolic compounds. Appl Environ Microbiol 54:3086–3091

    CAS  Google Scholar 

  • Bourbonnais R, Paice MG (1990) Oxidation of non-phenolic substrates: an expanded role of laccase in lignin biodegradation. FEBS Lett 267:99–102

    Article  CAS  Google Scholar 

  • Boyle CD (1998) Nutritional factors limiting the growth of Lentinula edodes and other white-rot fungi in wood. Soil Biol Biochem 30(6):817–823

    Article  CAS  Google Scholar 

  • Buswell JA, Chang ST (1993) Edible mushrooms: attributes and applications. In: Chang ST, Bushwell JA, Miles PG (eds) Genetics and breeding of edible mushrooms. Gordon and Bearch Scientific Publishers, Philadelphia, pp 297–324

    Google Scholar 

  • Buswell JA, Cai YJ, Chang ST (1996) Ligninolytic enzyme production and secretion in edible mushroom fungi. In: Royse DJ (ed) Mushroom biology and mushroom products. Penn State University, Pennsylvania, pp 113–122

    Google Scholar 

  • Cavallazzi JRP, Brito MS, Oliveira MGA, Villas-Bôas SG, Kasuya MCM (2004) Lignocellulolytic enzymes profile of three Lentinula edodes (Berk.) Pegler strains during cultivation on eucalyptus bark-based medium. Food Agr Env 2(1):291–297

    CAS  Google Scholar 

  • Chang ST (2006) The world mushroom industry: trends and technological development. Int J Med Mushrooms 8(4):297–314

    Article  Google Scholar 

  • Chiu SW, Law SC, Ching ML (2000) Themes for mushroom exploitation in the 21st century: sustainability, waste management, and conservation. J Gen Appl Microbiol 46:269–282

    Article  CAS  Google Scholar 

  • Di Lena G, Vivanti V, Quaglia GB (1997) Amino acid composition of wheat milling by-products after bioconversion by edible mycelia. Nahrung 41(5):285–288

    Article  CAS  Google Scholar 

  • Di Mario F, Rapanä P, Tomati U, Galli E (2008) Chitin and chitosan from basidiomycetes. Int J Biol Macromol 43:8–12

    Article  CAS  Google Scholar 

  • Diehle DA, Royse DJ (1986) Shiitake cultivation on sawdust: evaluation of selected genotypes for biological efficiency and mushroom size. Mycologia 78(6):929–933

    Article  Google Scholar 

  • Dill I, Kraepelin G (1988) Der Abbau von lignin/cellulose durch weissfäule-pilze: Einfluss spezifischer ökologischer faktoren. Forum Mikrobiol 11(88):484–489

    CAS  Google Scholar 

  • Elisashvili V, Penninckx M, Kachlishvili E, Tsiklauri N, Metreveli E, Kharziani T, Kvesitadze G (2008) Lentinus edodes and Pleurotus species lignocellulolytic enzymes activity in submerged and solid-state fermentation of lignocellulosic wastes of different composition. Biores Technol 99:457–462

    Article  CAS  Google Scholar 

  • Fan L, Soccol CR (2005) Coffee residues. In: Gush R (ed) Mushroom growers’ handbk 2. Mush World, Seoul, pp 92–95

    Google Scholar 

  • Gaitán-Hernández RG, Esqueda M, Gutiérrez A, Sánchez A, Beltrán-Gárcia M, Mata G (2006) Bioconversion of agrowastes by Lentinula edodes: the high potential of viticulture residues. Appl Microbiol Biotechnol 71:432–439

    Article  Google Scholar 

  • Ghorai S, Banik SP, Verma D, Chowdhury S, Mukherjee S, Khowala S (2009) Fungal biotechnology in food and feed processing. Food Res Int 42:577–587

    Article  CAS  Google Scholar 

  • Gilardi G, Abis L, Cass AEG (1995) Carbon-13 CP/MAS solid-state NMR and FT-IR spectroscopy of wood cell wall biodegradation. Enzyme Microb Technol 17(3):268–275

    Article  CAS  Google Scholar 

  • Harkin JM, Obst JR (1973) Syringaldazine, an effective reagent for detecting laccase and peroxidase in fungi. Experientia 29(4):381–508

    Article  CAS  Google Scholar 

  • Haw JF, Maciel GE, Schroeder HA (1984) C-13 nuclear magneticresonance spectrometric study of wood and wood pulping with cross polarization and magic-angle spinning. Anal Chem 56:1323–1329

    Article  CAS  Google Scholar 

  • Israilides C, Kletsas D, Arapoglou D, Philippoussis A, Pratsinis H, Ebrgerova A (2008) Cytostatic and immunomodulatory properties of the medicinal mushroom Lentinula edodes. Phytomedicine 15:512–519

    Article  CAS  Google Scholar 

  • Kaal EE, Field JA, Joyce TW (1995) Increasing lignolytic enzyme activities in several white-rot basidiomycetes by nitrogen-sufficient media. Bioresour Technol 53:133–139

    Article  CAS  Google Scholar 

  • Kachlishvili E, Penninckx MJ, Tsiklauri N, Elisashvili V (2005) Effect of nitrogen source on lignocellulolytic enzyme production by white-rot basidiomycetes under solid-state cultivation. World J Microbiol Biotechnol 22(4):391–397

    Article  Google Scholar 

  • Kalberer PP (1995) An investigation of the incubation phase of a shiitake (Lentinus edodes) culture. Mushroom Sci 14:375–383

    CAS  Google Scholar 

  • Kalberer PP (2000) Influence of urea and ammonium chloride on crop yield and fruit body size of shiitake (Lentinula edodes). Mushroom Sci 15:361–366

    CAS  Google Scholar 

  • Lakhtar H, Ismaili-Alaoui M, Philippoussis A, Macarie H, Roussos S (2007) Preliminary studies on Lentinula edodes strains able to degrade polyphenols in olive wastewater. In: XVI Nat bioprocess symposium—SINAFERM 2007, Curitiba

  • Lakhtar H, Ismaili-Alaoui M, Philippoussis A, Perraud-Gaime I, Roussos S (2010) Screening of strains of Lentinula edodes grown on model olive mill wastewater in solid and liquid state culture for polyphenol biodegradation. Int Biodet Biodeg 64(3):167–172

    Article  CAS  Google Scholar 

  • Leatham GF (1985) Extracellular enzymes produced by the cultivated mushroom Lentinus edodes during degradation of a lignocellulosic medium. Appl Environ Microbiol 50:859–867

    CAS  Google Scholar 

  • Leatham GF, Kirk TK (1983) Regulation of ligninolytic activity by nutrient nitrogen in white-rot basidiomycetes. FEMS Microbiol Lett 16:65–67

    Article  CAS  Google Scholar 

  • Lin Z (2005) Grass. In: Gush R (ed) Mushroom growers’ handbk 2. Mush World, Seoul, pp 96–99

    Google Scholar 

  • Lomberh ML, Solomko EF, Buchalo AS, Kirchhoff B (2002) Studies of medicinal mushrooms in submerged cultures. In: Sánchez JE, Huerta G, Montiel E (eds) Mushroom biology and mushroom products. UAEM, Cuernavaca, pp 367–377

    Google Scholar 

  • Makkar RS, Tsuneda A, Tokuyasu K, Mori Y (2001) Lentinula edodes produces a multi-component protein complex containing manganese (II)-dependent peroxidase, laccase and beta-glucosidase. FEMS Lett 200:175–179

    CAS  Google Scholar 

  • Mandels M, Andreotti R, Roche C (1976) Measurement of saccharifying cellulase. Biotechnol Bioeng Symp 6:21–33

    CAS  Google Scholar 

  • Massiot D, Fayon F, Capron M, King I, Le Calvé S, Alonso B, Durand J-O, Bujoli B, Gan Z, Hoatson G (2002) Modeling one- and two-dimensional solid state NMR spectra. Magn Reson Chem 40:70–76

    Article  CAS  Google Scholar 

  • Mata G, Savoie JM (1998) Extracellular enzyme activities in six Lentinula edodes strains during cultivation in wheat straw. World J Microbiol Biotechnol 14:513–519

    Article  CAS  Google Scholar 

  • Mata G, Savoie JM (2005) Whet straw. In: Gush R (ed) Mushroom growers’ handbk 2. Mush World, Seoul, pp 105–109

    Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugars. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  • Montini RMC, Passos JRS, Eira AF (2006) Digital monitoring of mycelium growth kinetics and vigor of shiitake (Lentinula edodes (Bergk.) Pegler) on agar medium). Braz J Microbiol 37:90–95

    Article  Google Scholar 

  • Moyson E, Verachtert H (1991) Growth of high fungi on wheat straw and their impact on the digestibility of the substrate. Appl Microbiol Biotechnol 36:421–424

    Article  CAS  Google Scholar 

  • Nikitina VE, Tsivileva OM, Pankratov AN, Bychkov A (2007) Lentinula edodes biotechnology—from lentinan to lectins. Food Technol Biotechnol 45(3):230–237

    CAS  Google Scholar 

  • Oei P (2003) Mushroom cultivation. In: Oei P (ed) Appropriate technology for mushroom growers, CTA, 3rd edn. Backhuys Publishers, Leiden, pp 1–7

    Google Scholar 

  • Ohga S (1992) Comparison of extracellular enzyme activities among different strains of Lentinus edodes grown on sawdust-based cultures in relationship to their fruiting abilities. J Jpn Wood Res Soc 38:310–316

    CAS  Google Scholar 

  • Ohga S, Royse DJ (2001) Transcriptional regulation of laccase and cellulose genes during growth and fruiting of Lentinula edodes on supplemented sawdust. FEMS Microbiol Lett 201:111–115

    Article  CAS  Google Scholar 

  • Ohga S, Cho NS, Thurston CF, Wood DA (2000) Transcriptional regulation of laccase and cellulase in relation to fruit body formation in the mycelium of Lentinula edodes on a sawdust-based substrate. Mycoscience 41:149–153

    Article  CAS  Google Scholar 

  • Okano K, Iida Y, Samsuri M, Prasetya B, Usagawa T, Watanabe T (2006) Comparison of in vitro digestibility and chemical composition among sugarcane bagasses treated by four white-rot fungi. Anim Sci J 77:308–313

    Article  CAS  Google Scholar 

  • Özçelik E, Pekşen A (2007) Hazelnut husk as a substrate for the cultivation of shiitake mushroom (Lentinula edodes). Biores Technol 98:2652–2658

    Article  Google Scholar 

  • Panichajakul S, Yindeeyoungyeon W, Triratana S (1991) Alteration of laccases and acid phosphatase in mono-and dikaryotic mycelia of Lentinus edodes. In: Maher MJ (ed) Science and cultivation of edible fungi. Balkema, Rotterdam, pp 241–249

    Google Scholar 

  • Pereira Júnior JA, Correia MJ, Oliveira NT (2003) Cellulase activity of a Lentinula edodes (Berk.) Pegl. strain grown in media containing carboximetilcellulose or microcrystalline cellulose. Braz Arch Biol Technol 46(3):333–337

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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(2):191–200

    Article  CAS  Google Scholar 

  • Philippoussis A, Diamantopoulou P, Zervakis G (2002) Monitoring of mycelium growth and fructification of Lentinula edodes on several agricultural residues. In: Sánchez JE, Huerta G, Montiel E (eds) Mushroom biology and mushroom products. UAEM, Cuernavaca, pp 279–287

    Google Scholar 

  • 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(6):551–557

    Article  Google Scholar 

  • Philippoussis A, Diamantopoulou P, Israilides C (2007a) Productivity of agricultural residues used for the cultivation of the medicinal fungus Lentinula edodes. Int Biodeterior Biodegrad 59(3):216–219

    Article  CAS  Google Scholar 

  • Philippoussis A, Diamantopoulou P, Kokkinis G, Kazoglou Y, Parisopoulos G (2007b) Potential use of littoral vegetation residues from Lake Mikri Prespa, as substrate for mushrooms cultivation. In: Proceedings of international conference on environment management, engineering, planning and economics (CEMEPE 2007), Skiathos, pp 1663–1669

  • Pire DG, Wright JE, Alberto E (2001) Cultivation of shiitake using sawdust from widely available local woods in Argentina. Micol Apl Int 13(2):87–91

    Google Scholar 

  • Ride JP (1980) The effect of induced lignification on the resistance of wheat cell walls to fungal degradation. Physiol Plant Pathol 16:187–196

    Article  CAS  Google Scholar 

  • Ride JP, Drysdale RB (1972) A rapid method for the chemical estimation of filamentous fungi in plant tissue. Physiol Plant Pathol 2:7–15

    Article  CAS  Google Scholar 

  • Rigas F, Papadopoulou K, Philippoussis A, Papadopoulou M, Chatzipavlidis J (2009) Bioremediation of lindane contaminated soil by landfarming technology. Water Air Soil Pollut 197:121–129

    Article  CAS  Google Scholar 

  • Rossi IH, Monteiro AC, Machado JO (2003) Shiitake Lentinula edodes production on a sterilized bagasse substrate enriched with rice bran and sugarcane molasses. Braz J Microbiol 34:66–71

    Google Scholar 

  • Royse DJ (2004) Specialty mushrooms, mushroom fact sheet. Mushroom Spawn Laboratory, Penn State University, Pennsylvania

    Google Scholar 

  • Royse DJ, Bahler CC (1986) Effects of genotype, spawn run time and substrate formulation on biological efficiency of shiitake. Appl Environ Microbiol 52(6):1425–1427

    CAS  Google Scholar 

  • Royse DJ, Sánchez JE (2007) Ground wheat straw as a substitute for portions of oak wood chips used in Shiitake (Lentinula edodes) substrate formulae. Biors Technol 98:2137–2141

    Article  CAS  Google Scholar 

  • Royse DJ, Sanchez-Vazquez JE (2001) Influence of substrate wood-chip particle size on shiitake (Lentinula edodes) yield. Biores Technol 76:229–233

    Article  CAS  Google Scholar 

  • Salmones D, Mata G, Ramos LM, Waliszewski KN (1999) Cultivation of shiitake mushroom, Lentinula edodes in several lignocellulosic materials originating from the subtropics. Agron 19(1):13–19

    Article  Google Scholar 

  • Scotti CT, Vergoignan C, Feron G, Durand A (2001) Glucosamine measurement as indirect method for biomass estimation of Cunninghamella elegans grown in solid state cultivation conditions. Biochem Eng J 7:1–5

    Article  CAS  Google Scholar 

  • Silva EM, Machuca A, Milagres AMF (2005a) Effect of cereal brans on Lentinula edodes growth and enzyme activities during cultivation on forestry waste. Lett Appl Microbiol 40:283–288

    Article  CAS  Google Scholar 

  • Silva EM, Machuca A, Milagres AMF (2005b) Evaluating the growth and enzyme production from Lentinula edodes strains. Process Biochem 40:161–164

    Article  CAS  Google Scholar 

  • Silva ÉS, Cavallazzi JRP, Muller G (2007) Biotechnological applications of Lentinus edodes. J Food Agric Environ 5(3&4):403–407

    CAS  Google Scholar 

  • Smith JE, Rowan NJ, Sullivan R (2002) Medicinal mushrooms: a rapidly developing area of biotechnology for cancer therapy and other bioactivities. Biotechnol Lett 24:1839–1845

    Article  CAS  Google Scholar 

  • Song CH, Chow KY (1987) A synthetic medium from the production of submerged cultures of Lentinus edodes. Mycol 79:866–876

    Article  Google Scholar 

  • Srijumpa N (2003) Use of grasses as a substrate for the cultivation of oyster mushroom. Food and Fertilizer Technology Center (FFTC), Taipei

    Google Scholar 

  • Wasser S (2002) Medicinal mushroom as a source of antitumor and immunomodulating polysaccharides. Appl Microbiol Biotechnol 60:258–274

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors acknowledge financial support given partially by the General Secretariat of Research and Technology through the 05 PAV 105 project and partially by the Institute of Agricultural Engineering of the National Agricultural Research Foundation (NAGREF). They also thank Dr. Y. Kazoglou, (Society for the Protection of Prespa) for providing the raw substrate material and Dr. C. Mountzouris (Agricultural University of Athens) for helping in raw material processing.

Author information

Authors and Affiliations

  1. Laboratory of Edible and Medicinal Fungi, National Agricultural Research Foundation, IAMC, 61 Democratias St., Ag. Anargyri Attikis, 13561, Athens, Greece

    A. Philippoussis, P. Diamantopoulou & G. Parissopoulos

  2. School of Chemical Engineering, National Technical University of Athens, 15700, Athens, Greece

    K. Papadopoulou

  3. IRD, Unité 185 Biotrans, IMEP Case 441, FST Saint Jérôme, Université Paul Cézanne, Av. Escadrille Normandie-Niemen, 13397, Marseille cedex 20, France

    H. Lakhtar & S. Roussos

  4. Department of Food Science and Technology, Laboratory of Food Microbiology and Biotechnology, Agricultural University of Athens, Iera Odos 75, 11855, Athens, Greece

    S. Papanikolaou

Authors
  1. A. Philippoussis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Diamantopoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. Papadopoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. H. Lakhtar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. Roussos
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. G. Parissopoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. S. Papanikolaou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. Philippoussis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Philippoussis, A., Diamantopoulou, P., Papadopoulou, K. et al. 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 (2011). https://doi.org/10.1007/s11274-010-0458-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11274-010-0458-8

Keywords

Search

Navigation