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Production of Extracellular Enzymes and Degradation of Biopolymers by Saprotrophic Microfungi from the Upper Layers of Forest Soil

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Production of Extracellular Enzymes and Degradation of Biopolymers by Saprotrophic Microfungi from the Upper Layers of Forest Soil Plant Soil (2011) 338:111–125 DOI 10.1007/s11104-010-0324-3 REGULAR ARTICLE Production of extracellular enzymes and degradation of biopolymers by saprotrophic microfungi from the upper layers of forest soil Petr Baldrian & Jana Voříšková & Petra Dobiášová & Věra Merhautová & Ludmila Lisá & Vendula Valášková Received: 14 October 2009 /Accepted: 10 February 2010 /Published online: 26 February 2010 # Springer Science+Business Media B.V. 2010 Abstract Production of extracellular enzymes partic- The microfungal strains were able to produce signif- ipating in the degradation of biopolymers was studied icant growth on a range of 41–87, out of 95 simple C- in 29 strains of nonbasidiomycetous microfungi containing substrates tested in a Biolog™ assay, isolated from Quercus petraea forest soil based on monosaccharides being for all strains the most rapidly the frequency of occurrence. Most of the isolates were metabolized C-sources. Comparison with saprotro- ascomycetes and belonged to the genera Acremonium, phic basidiomycetes from the same environment Alternaria, Cladosporium, Geomyces, Hypocrea, showed that microfungi have similar cellulolytic Myrothecium, Ochrocladosporium, and Penicillium capabilities and higher chitinase activities which (18 isolates), and two isolates were zygomycetes. Only testifies for their active role in the decomposition of six isolates showed phenol oxidation activity which both lignocellulose and dead fungal biomass, impor- was low and none of the strains were able to degrade tant pools of soil carbon. humic acids. Approximately half of the strains were able to degrade cellulose and all but six degraded Keywords Lignocellulose . Soil microfungi . Chitin . chitin. Most strains produced significant amounts of Enzymes . Decomposition . Forest biogeochemistry the cellulolytic enzymes cellobiohydrolase and β- glucosidase and the chitinolytic enzymes chitinase, Abbreviations chitobiosidase, and N-acetylglucosaminidase. The ABTS 2,2′-azinobis-3-ethylbenzothiazoline- highest cellulase activities were found in Penicillium 6-sulfonic acid strains, and the highest activity of chitinolytic enzymes AMC 7-aminomethyl-4-coumarin was found in Acremonium sp. The production of the CCBAS Culture Collection of Basidiomycetes hemicellulose-degrading enzymes α-galactosidase, β- ITS Internal Transcribed Spacer galactosidase, and α-mannosidase was mostly low. MEA Malt Extract Agar MnP Mn-peroxidase MUF 4-methylumbelliferol Responsible Editor: M. Francesca Cotrufo. P. Baldrian (*) : J. Voříšková : P. Dobiášová : V. Merhautová : L. Lisá : V. Valášková Laboratory of Environmental Microbiology, Introduction Institute of Microbiology of the ASCR, v.v.i., Vídeňská 1083, 14220 Praha 4, Czech Republic Biopolymers contained within the cell walls of plants e-mail: [email protected] and fungi represent the major source of carbon in 112 Plant Soil (2011) 338:111–125 forest soils entering the environment either with dead produce cellobiose from either reducing or nonreduc- plant material during litterfall or as a result of fungal ing ends. Ultimately, β-glucosidases cleave cellobiose growth. Actually, cellulose, lignin and chitin are the into two glucose molecules (Baldrian and Valášková three most abundant biopolymers in terrestrial biomes 2008). However, the ability to produce the individual and the transformation of carbon present within thus components of this cellulolytic system varies among represents an important process in the C-cycle. cellulolytic fungi (Baldrian and Valášková 2008; Lynd Saprotrophic soil fungi are often considered to be et al. 2002). the most efficient decomposers of these biopolymers Chitin is the most important biopolymer in soils that (Kjoller and Struwe 2002; Baldrian 2008a) and some does not originate in the plant biomass. Full chitin authors hypothesize that fungi actually dominate hydrolysis is typically performed by a three component certain decomposition niches (de Boer et al. 2005). system consisting of endochitinase, chitobiosidase, and While this seems to be justified for ligninolytic wood- N-acetylglucosaminidase. Endochitinases cleave in the associated fungi that have been largely characterized middle of the chitin chain while the chitobiosidase due to the biotechnology-related research (Hatakka (exochitinase) releases chitooligosaccharides from the 2001; Baldrian 2008b) and for the same reason the end of the polymer chain. N-acetylglucosaminidase production of cellulases is well understood in certain catalyzes the release of terminal, non-reducing N- fungi, e.g., Trichoderma (Hypocrea) spp. (Lynd et al. acetylglucosamine residues from chitin, with the highest 2002), the abilities of several common groups of soil- efficiency in cleaving the dimer diacetylchitobiose. inhabiting fungi are not well-characterized in this Recent genome sequencing data show that the genomes respect. Only recently, saprotrophic basidiomycetes of filamentous fungi typically contain between 10 and living in forest soil and litter have been characterized 25 different chitinases, compared to only two to four in with respect to the production of cellulose, hemicel- bacteria (Seidl 2008). This diversity indicates an lulose, and lignin-degrading enzymes (Steffen et al. important role of this group of fungi in chitin 2000, 2007; Valášková et al. 2007). However, the transformation in soils as well as the promise for a potential of nonbasidiomycetous microfungi, another future use in biotechnology. important group of soil and litter-associated fungi to The aim of this work was to describe the production attack biopolymers in soil or litter, remains largely of extracellular enzymes by nonbasidiomycetous micro- unexplored. Unlike ectomycorrhizal fungi, where fungi isolated from forest soil. Although saprotrophic biodegradative enzyme activities seem to be limited basidiomycetes are capable to decompose litter more (Baldrian 2009a), several microfungi are typical rapidly than nonbasidiomycetous fungi (Osono 2007; saprotrophs that produce biopolymer-degrading Osono and Takeda 2006), litter decomposing in situ enzymes (Bhiri et al. 2008; Hayashi et al. 1997; Lynd differs significantly from the litter decomposed by et al. 2002; Mamma et al. 2008). basidiomycetes only (Valášková et al. 2007). This In contrast to lignin decomposition which seems to be indicates an important role for nonbasidiomycetous exclusively performed by saprotrophic basidiomycetes fungi in its degradation. We wanted to answer the (Baldrian 2008a), degradation of polysaccharides— following questions: cellulose, hemicelluloses and chitin—is performed by (1) How do the microfungi potentially contribute to many nonbasidiomycetous fungi (Chavez et al. 2006; the degradation of cellulose, chitin, and lignin? Lynd et al. 2002; Seidl 2008). The degradation of (2) What simple carbon compounds are they able to cellulose as both the most abundant and rapidly use as substrates for growth? Is the utilization of utilizable biopolymer of plant litter now attracts consid- cellulose- and chitin-derived monomers related erable attention with respect to the understanding of the to the ability of individual strains to perform rates of carbon cycle-related processes (Sinsabaugh et cellulose and chitin decomposition? al. 2008). The estimation of cellulose degradation (3) Can a general conclusion be made on the extracel- potential by a group of commonly occurring soil lular enzyme production by nonbasidiomycetous microorganisms is thus important. Cellulose degrada- microfungi compared to basidiomycetes? tion is typically performed by the concerted action of three classes of enzymes. Endocellulases cleave in the To answer these questions, we isolated strains of middle of the cellulose chains while the exocellulases nonbasidiomycetous fungi in the Quercus petraea Plant Soil (2011) 338:111–125 113 forest, in the same site where we previously studied All strains of litter-decomposing basidiomycete litter degradation by isolates of saprotrophic basidio- fungi (Collybia maculata CCBAS 755, Flammulina mycetes (Valášková et al. 2007)andwherethe velutipes CCBAS 363, Gymnopus ocior CCBAS 287, activity of several enzymes active in biopolymer Hypholoma fasciculare CCBAS 283, Lepista nuda degradation was detected in situ (Šnajdr et al. 2008). CCBAS 136, Marasmius quercophilus CCBAS 290, Mycena galopus CCBAS 139, Mycena pura CCBAS 280, Mycena rubromarginata CCBAS 299, Mycena Materials and methods viridimarginata CCBAS 134, Pholiota flammans CCBAS 229, Rhodocollybia butyracea CCBAS 286, Study site, strain isolation and maintenance Stropharia hornemannii CCBAS 295, Stropharia semiglobata CCBAS 144) were obtained from the Thefungiwereisolatedfromanoak(Quercus Culture Collection of Basidiomycetes of the Institute petraea) forest floor (L and H horizons) in the of Microbiology of the ASCR, v.v.i. (Prague, Czech Xaverovský Háj Natural Reserve, near Prague, Czech Republic). The strains CCBAS 280, CCBAS 283, Republic. The soil was an acidic cambisol (inceptisol) CCBAS 286, and CCBAS 287 were previously with developed L, H, Ah and A horizons: L— isolated from the same site as the microfungi thickness 0.5–1.5 cm, pH 4.3; 46.2% C; 1.76% N; (Valášková et al. 2007), while the other species were H—thickness 1.5–2.5 cm, pH 3.7; 21.5% C; 0.56% selected based on the observations of fruitbodies at N. High, but spatially variable activity of extracellular the same site or at other Quercus petraea forest sites ligninolytic and hydrolytic enzymes was found in the in Central Europe. Fungal strains were maintained on
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