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Laboratory of Forest Ecology, Graduate School of Agriculture, Kyoto University, Kyoto 606-8520, Japan
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ABSTRACT |
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The effect of litter type and incubation temperature on the ability of fungi to decompose leaf litter of subalpine trees was examined by a pure-culture test. Mass loss of Abies needle and Betula leaf litter and utilization patterns of lignin and carbohydrates were investigated under two temperature conditions (20 C and 10 C) and compared for 29 species in basidiomycetes, ascomycetes and zygomycetes. The decomposing ability was generally higher in basidiomycetes than in ascomycetes and zygomycetes. Mass loss (% original mass) of litter was higher in Betula than in Abies and higher at 20 C than at 10 C. The 29 fungi were divided into lignocellulose decomposers, cellulose decomposers and sugar fungi based on their substrate utilization in Abies and Betula litter. Mass loss of lignin and carbohydrates by lignocellulose and cellulose decomposers was higher in Betula than in Abies. Mass loss of carbohydrates was higher at 20 C than at 10 C, but the temperature did not influence mass loss of lignin, indicating lignin decomposition by fungi was less sensitive to temperature than carbohydrate decomposition. Lignin/ carbohydrate loss ratio (L/C) of Collybia spp. that caused selective delignification was lower at 20 C than at 10 C. These results indicate that the decomposability of litter, lignin and carbohydrate was different between Abies and Betula and that temperature affected not only the rate at which fungi decompose litter but also the ability of fungi to use lignin and carbohydrates.
Key words: birch, carbohydrate, fir, fungi, lignin, subalpine coniferous forest
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) because they decompose the lignocellulose matrix in litter that other organisms are unable to decompose (Kjøller and Struwe 1982, Cooke and Rayner 1984). The abilities of fungi to decompose leaf litter have been examined by pure-culture tests (reviewed in Osono et al 2003; Osono 2003; Koide et al 2005a, b). These studies showed that fungi were divided into three functional groups based on their substrate utilization. Lignocellulose decomposers attack both lignin and carbohydrates in various proportions, which result in a significant mass loss of litter. Cellulose decomposers preferentially attack carbohydrates with a slight or negligible loss of lignin. Sugar fungi rely on soluble sugars and are unable to disolve the structural polymers.
Subalpine forests in temperate area of the northern hemisphere are characterized by slow decomposition and high accumulation of soil organic matter (Edmonds 1984; Zech et al 1990; Tian et al 1997, 2000; Prichard et al 2000). This has been attributed to lower resource quality of leaf litter of dominant conifers such as Abies than in broadleaf trees such as Betula (Vogt et al 1980, Stump and Binkley 1993, Tian et al 2000). The relative increase of lignin content in decomposed materials, which was attributable to the faster decomposition of holocellulose than lignin decomposition by decomposer communities (Tian et al 2000), also will contribute to the accumulation of recalcitrant soil organic matter (Takeda 1998). However few studies have been conducted regarding the potential ability of diverse fungi to decompose holocellulose and lignin in subalpine leaf litter and the effect of resource quality between litter types on fungal decomposition.
The reduced activity of fungi to decompose litter under relatively low temperature is another responsible factor (Bisset and Parkinson 1980, Taylor and Jones 1990, Nakatsubo et al 1997, Reichstein et al 2000, Uchida et al 2000, Gonzalez and Seastedt 2001). Tian et al (2000) found that decomposition of holocellulose and lignin showed a clear seasonal pattern, which was faster in summer than in other seasons. These indicate the necessity to study the response of fungal decomposition to temperature, but the effects of temperature on the ability of fungi to decompose leaf litter are not well known (Thormann et al 2004).
In this study we investigated and compared the ability of 29 fungal species in the basidiomycota, ascomycota and zygomycota to decompose subalpine leaf litter. Abies needle and Betula leaf litter were used as materials. Abies needle litter was characterized by lower resource quality to fungi (i.e. higher lignin content and lower nutrient contents, than Betula leaf litter [Tian et al 1998]). Incubation was done under two temperature conditions (20 C and 10 C) that represented the uppermost and intermediate values, respectively, of temperature range during the snow-free growing season when litter decomposition occurs most actively in a subalpine forest (Tian et al 2000). Fifteen of the 29 test fungi that showed marked ability to decompose litter were examined further for their ability to decompose lignin and holocellulose in litter. Fungi were isolated either from sporocarps or decomposing leaves collected in a subalpine coniferous forest in central Japan or obtained also from culture collections.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Fomes fomentarius and two unidentified basidiomycete species coded B822 and PI1027 were obtained from basidiocarps occurring on dead wood on a study site in the subalpine Abies-Betula forest on Mount Ontake, Gifu, central Japan in Oct 2000. The study site is 2050 m a.s.l. Mean annual temperature is approximately 2 C and annual precipitation is approximately 2500 mm. Further details of the site were described in Mori et al (2004). The other nine basidiomycetes were obtained from a culture collection (IFO/NBRC, Chiba, Japan). Mycena polygramma, Collybia dryophila, Collybia butyracea, and Collybia peronata (litter decomposing basidiomycetes), and Trametes versicolor, Kuehneromyces mutabilis, Laetiporus sulphureus, Fomitopsis pinicola, Fuscoporia obliqua, and Fomes fomentarius (wood decomposing basidiomycetes) were common in subalpine forests (Imazeki et al 1987, Takahashi 1991). Mycena polygramma, three Collybia species, T. versicolor, and L. sulphureus also were used in the previous decomposition tests (Osono and Takeda 2002a, b, 2003; Osono et al 2003; Fukasawa et al 2005). Wood-decomposing fungi were used in the present study because some of them have vigorous ability to decompose lignin and (or) cellulose in plant residues (Eriksson et al 1990, Worrall et al 1997) and would be useful to evaluate the effects of litter type and incubation temperature on lignocellulose decomposition. Most of the ascomycete and zygomycete strains were isolated from Abies needles and Betula leaf litter collected from the subalpine forest floor in Jun, Aug and Oct 2000 by means of the washing method according to Osono and Takeda (2001b). Discosia atrocreas was obtained from the culture collection (IFO/NBRC). Truncatella augustata, Chalara longipes, Aureobasidium pullulans and Tysanophora penicillioides occurred frequently on Abies needles (Aoki et al 1990, Iwamoto and Tokumasu 2001, Iwamoto unpublished data) and these strains were provided from the culture collection of Dr S. Iwamoto (Tsukuba University, Japan).
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Decomposition test.— –
Abies needle or Betula leaf litter (0.5 g) was sterilized by exposure to ethylene oxide gas at 60 C for 6 h. The sterilized litter was placed on the surface of Petri dishes (9 cm diam) containing 20 mL 2% agar. Inocula for each assessment were cut out of the margin of the previously inoculated Petri dishes on 2% malt-extract agar (malt extract 2% and agar 2% [w/v]) with a sterile cork borer (6 mm diam) and placed on the agar adjacent to the leaves, one plug per plate. The plates were incubated 3 mo at 20 C or 10 C in the dark. The plates were sealed firmly with laboratory film during incubation so that moisture did not limit decomposition on the agar. After incubation the leaves were retrieved, oven-dried at 40 C 1 wk and weighed. The initial litter also was sterilized, oven-dried at 40 C 1 wk and weighed to determine original mass. Mass loss of litter was determined as a percentage of the original mass. Four plates were prepared for each isolate, and four un-inoculated plates served as a control. The duplicated leaves then were combined and used for chemical analyses as describe below. The incubation regimes of 20 C and 10 C adopted in this study represented the uppermost and intermediate values, respectively, of temperature range during the snow-free growing season (May–Oct) when litter decomposition occurred most actively in the subalpine site (Tian et al 2000).
Chemical analyses.— –
Litter samples were ground in a laboratory mill (0.5 mm screen). The amount of lignin in the samples was estimated by means of gravimetry, using hot sulfuric acid digestion (King and Heath 1967). Samples were extracted with alcohol-benzene at room temperature (15–20 C), and the residue was treated with 72% sulfuric acid (v/v) for 2 h at room temperature with occasional stirring. The mixture was diluted with distilled water to make a 2.5% sulfuric acid solution and autoclaved at 120 C for 60 min. After cooling the residue was filtered and washed with water through a porous crucible (G4), dried at 105 C and weighed as acid-insoluble residue. The filtrate (autoclaved sulfuric acid solution) was used for total carbohydrate analysis. The amount of carbohydrate in the filtrate was estimated by means of the phenol-sulfuric acid method (Dubois et al 1956). A total of 1 mL of 5% phenol (v/v) and 5 mL of 98% sulfuric acid (v/v) were added to the filtrate. The optical density of the solution was measured by a spectrophotometer at 490 nm, using known concentrations of D-glucose as standards. Total N content was measured by automatic gas chromatography (NC analyzer SUMIGRAPH NC-900, Sumitomo Chemical Co., Osaka, Japan).
Lignin/carbohydrate loss ratio (L/C) is a useful index of substrate-use pattern of each fungal species (Osono and Takeda 2002b, Osono et al 2003). L/C of each fungal species was calculated according to the equation:
Statistical analysis.— –
Two-way ANOVA was performed for 15 of 29 species to evaluate the difference in mass loss of litter using litter type (Abies and Betula) and incubation temperature (20 C and 10 C) as independent variables. Two-way ANOVA also was performed for a further five of the 15 species to evaluate the difference in mass loss of lignin and carbohydrates using litter type and incubation temperature as independent variables. Methods are described in Osono et al (2003).
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RESULTS |
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Mass loss of litter.— –
Abies needle litter loss ranged from –0.8% to 13.8% at 20 C and from –2.6% to 8.3% at 10 C and that of Betula leaf litter ranged from –2.5% to 44.1% at 20 C and from –2.5% to 30.5% at 10 C (TABLE I
). Mass loss was generally higher in Betula than in Abies, higher at 20 C than at 10 C and higher in litter decomposed by basidiomycetes than by ascomycetes and zygomycetes.
The results of two-way ANOVA indicated that mass loss of litter for the 15 selected species was significantly higher in Betula than in Abies and higher at 20 C than at 10 C (TABLE II).
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). Mass loss of lignin in Abies ranged from –4.2% to 36.0% at 20 C and from 0.9% to 13.3% at 10 C and that in Betula ranged from –1.9% to 72.8% at 20 C and from –0.4% to 32.9% at 10 C. Mass loss of carbohydrate in Abies ranged from 2.5% to 16.6% at 20 C and from 0.0% to 13.2% at 10 C and that in Betula ranged from 2.3% to 66.8% at 20 C and from 6.4% to 48.1% at 10 C. Mass loss of lignin and carbohydrates was generally higher in Betula than in Abies and higher at 20 C than at 10 C. Mass loss of lignin was higher in litter decomposed by basidiomycetes than by ascomycetes, whereas that of carbohydrates was not markedly different between basidiomycetes and ascomycetes.
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). Mass loss of carbohydrates for the five selected species was also significantly higher in Betula than in Abies and significantly but only marginally higher at 20 C than at 10 C (TABLE II).
Substrate use.— –
L/C in Abies ranged from –0.5 to 3.2 at 20 C and from 0.2 to 0.7 at 10 C (TABLE III). Collybia dryophila caused undetectable mass loss of carbohydrates in Abies so that L/C was not calculated. L/C in Betula ranged from –0.1 to 21.3 at 20 C and from 0.0 to 5.2 at 10 C. Collybia species (C. dryophila, C. butyracea, C. peronata) generally had high L/C values showing selective delignification. Mycena polygramma, T. versicolor, basidiomycete B822 and K. mutabilis showed simultaneous decomposition of lignin and carbohydrates and (or) greater decomposition of carbohydrates than lignin. Laetiporus sulphureus, basidiomycete PI1027 and six ascomycete species showed selective loss of carbohydrates with negligible mass loss of lignin.
L/C of M. polygramma, K. mutabilis, C. peronata and Discosia atrocrea was lower in Abies than in Betula, whereas L/C of C. butyracea and Trichoderma viride was higher in Abies than in Betula. L/C of C. dryophila, T. versicolor, L. sulphureus, basidiomycete PI1027 and Geniculosporium sp.2 were not markedly different between Abies and Betula.
L/C of Collybia dryophila was lower (i.e. this fungus decomposed lignin in preference to carbohydrates, less so at 20 C than at 10 C both in Abies and Betula) whereas, L/C of M. polygramma, T. versicolor, K. mutabilis and Geniculosporium sp.2 were not markedly different between 20 C and 10 C.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Osono et al 2003).
High rates of decomposition were limited to members of basidiomycetes such as M. polygramma, Collybia spp., T. versicolor and K. mutabilis. These fungi were regarded as lignocellulose decomposers of Abies needle and Betula leaf litter. They also have shown an ability to decompose both lignin and carbohydrates in other litter types (Lindeberg 1946, Hering 1967, De-Boois 1976, Dix and Simpson 1984, Miyamoto et al 2000, Osono and Takeda 2002b, Osono et al 2003).
Laetiporus sulphureus, causing selective mass loss of carbohydrates in Abies and Betula, already has been reported as causing brown rot (Osono and Takeda 2003). Basidiomycete PI1027 also is regarded as cellulose decomposing fungi. Geniculosporium sp.2, D. atrocreas, T. augustata, P. neglecta, T. viride and P. glabrum in ascomycetes also are regarded as cellulose decomposers of Abies and Betula. Species in Geniculosporium, Discosia, Pestalotiopsis, Trichoderma and Penicillium are common litter inhabitants and have been shown to decompose carbohydrates in some litter types (Saito 1960, Hering 1967, Osono and Takeda 2002b, Osono et al 2003). These ascomycetes presumably caused soft-rot type decomposition in which carbohydrates were attacked preferentially (Nilsson et al 1989, Worrall et al 1997).
On the other hand other basidiomycetes, ascomycetes and zygomycetes caused negligible mass loss in Abies needle and Betula leaf litter. Some of these fungi, such as A. pullulans, C. cladosporioides, U. ramanniana and M. alpina, might be regarded as "sugar fungi" sensu Hudson (1968). The growth of these fungi may depend on readily available energy sources such as soluble carbohydrates. Trichoderma polysporum and Paecilomyces farinosus are parasitic fungi that have limited ability to decompose litter (Harney and Widden 1991, Osono and Takeda 2002b). Other fungi might have a limited ability to attack Abies and Betula litter or it may be that the cultural conditions in this study might have been unsuitable for their growth.
Lignin and carbohydrate utilization pattern.— –
Basidiomycetes attacked lignin and carbohydrates in Abies and Betula litter in various proportions, whereas ascomycetes preferentially decomposed carbohydrates. This result is consistent with Osono and Takeda (2002b), Osono et al (2003) and Fukasawa et al (2005), who compared lignin and cellulose decomposing ability among diverse fungi in other litter species or types. Collybia species (C. dryophila, C. butyracea, C. peronata) caused selective delignification in Abies and Betula. Lignin to carbohydrate loss ratio of Collybia in other litter types was determined as 2.2–8.2 (Lindeberg 1946, Osono and Takeda 2002b, Osono et al 2003). Collybia dryophila has been reported to produce laccase and manganese peroxidase (Hofrichter 2002, Tuomela et al 2005) and Collybia species has been known as white-rot decomposers in forest floor materials (Gourbière 1983, Miyamoto and Igarashi 2004). These indicated that Collybia spp. has an ability to cause selective delignification in various litter types. In these studies however the ligninolytic activity of Collybia spp. was evaluated as the loss of acid-insoluble "lignin" fractions during decomposition. Application of new analytical methodologies such as solid-state 13C nuclear magnetic resonance (NMR) to litter materials decomposed by Collybia spp. would provide further insight into their ligninolytic activity (Robert and Chen 1989, Almendros et al 1992).
Values of L/C for the other basidiomycetes in the present study are within the range of previous reports. Those of Mycena polygramma have been reported as 0.2–0.7, T. versicolor as 0.2–1.0 and L. sulphureus as 0–0.3 (Osono and Takeda 1999, 2002b, 2003; Osono et al 2003; Fukasawa et al 2005). Geniculosproium, Discosia and Trichoderma in ascomycetes have caused selective carbohydrate decomposition in beech litter with L/C of 0.1–0.3, according to Osono and Takeda (1999).
Effect of litter type.— –
Mass loss of litter, lignin and carbohydrates was greater in Betula leaf litter than in Abies needle litter. This difference in decomposability between Abies and Betula also has been reported in the field by Tian et al (2000). Mikola (1956) and Osono and Takeda (2001a) also have reported the effect of litter types on the ability of fungi to decompose lignin and carbohydrates in pure-culture decomposition tests. One possible explanation for this is the difference in resource quality between litter types. For example the content of nitrogen, one of essential macronutrients for fungal growth, was lower in Abies than in Betula, which may impede fungal growth in Abies needle litter. On the other hand the difference in the arrangement of fibers within cell walls and the accessibility of enzymes, the higher content of guaiacyl unit in gymnospermous lignin than angiospermous lignin or host specificity of individual fungal species may account for the difference in mass loss between Abies and Betula litter. The difference in the decomposability between Abies and Betula, as well as the substrate-dependent pattern of lignin and carbohydrate use for diverse fungal species, suggest that the changes in species composition of not only trees but also fungi potentially influence the accumulation of soil organic matter in subalpine forests.
Effect of temperature.— –
Mass loss of litter and carbohydrates was higher at 20 C than at 10 C but a similar difference was not detected in mass loss of lignin, suggesting lignin decomposition by the test fungi was less sensitive to temperature than carbohydrate decomposition within this temperature range. Such a difference in the response of lignin and carbohydrate decomposition to temperature resulted in the lower values of L/C at 20 C than at 10 C, which obviously was detected in C. dryophila (i.e. this fungus decomposed lignin in preference to carbohydrates, less so at 20 C than at 10 C). Donnelly et al (1990) measuring lignin and cellulose decomposition in soil incubated at 4 C, 12 C and 24 C found the lower ratio of lignin decomposition to cellulose decomposition at higher temperature. Therefore not only the rate at which fungi decompose litter but also the ability of fungi to use lignin and carbohydrate can be affected by temperature. Such a shift in fungal decomposition in lignin and cellulose in relation to temperature suggests the changing role of fungi in decomposition processes in subalpine forests in response to future increase of global temperature, leading to the increased accumulation of recalcitrant soil organic matter derived from lignin and lignin-like substances. It should be noted however that temperature increase also would be accompanied with the shift in species composition of basidiomycetes responsible for lignin and cellulose decomposition. Nevertheless the abundance and distribution of ligninolytic litter decomposing basidiomycetes on subalpine forest soils have been scarcely documented in published literature (Senn-Irlet and Bieri 1999). Further studies thus are required in this regard to discuss the role of ligninolytic fungi on the accumulation of soil organic matter in subalpine forests.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Corresponding author. E-mail: fujijun{at}kais.kyoto-u.ac.jp
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