Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers.

Organic matter decomposition in the globally widespread coniferous forests has an important role in the carbon cycle, and cellulose decomposition is especially important in this respect because cellulose is the most abundant polysaccharide in plant litter. Cellulose decomposition was 10 times faster in the fungi-dominated litter of Picea abies forest than in the bacteria-dominated soil. In the soil, the added (13)C-labelled cellulose was the main source of microbial respiration and was preferentially accumulated in the fungal biomass and cellulose induced fungal proliferation. In contrast, in the litter, bacterial biomass showed higher labelling after (13)C-cellulose addition and bacterial biomass increased. While 80% of the total community was represented by 104-106 bacterial and 33-59 fungal operational taxonomic units (OTUs), 80% of the cellulolytic communities of bacteria and fungi were only composed of 8-18 highly abundant OTUs. Both the total and (13)C-labelled communities differed substantially between the litter and soil. Cellulolytic bacteria in the acidic topsoil included Betaproteobacteria, Bacteroidetes and Acidobacteria, whereas these typically found in neutral soils were absent. Most fungal cellulose decomposers belonged to Ascomycota; cellulolytic Basidiomycota were mainly represented by the yeasts Trichosporon and Cryptococcus. Several bacteria and fungi demonstrated here to derive their carbon from cellulose were previously not recognized as cellulolytic.

[1]  W. Liesack,et al.  Bacterial populations and environmental factors controlling cellulose degradation in an acidic Sphagnum peat. , 2011, Environmental microbiology.

[2]  P. Baldrian,et al.  Enzyme activities of fungi associated with Picea abies needles , 2011 .

[3]  M. Gryndler,et al.  Local distribution of ectomycorrhizae-associated basidiomycetes in forest soil correlates with the degree of soil organic matter humification and available electrolytes , 2010, Folia Microbiologica.

[4]  R. Knight,et al.  Rapid denoising of pyrosequencing amplicon data: exploiting the rank-abundance distribution , 2010, Nature Methods.

[5]  P. Gerhardt,et al.  Methods for general and molecular bacteriology , 1994 .

[6]  Robert C. Edgar,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2001 .

[7]  J. Cairney,et al.  Influence of repeated prescribed burning on incorporation of 13C from cellulose by forest soil fungi as determined by RNA stable isotope probing , 2009 .

[8]  W. Boer,et al.  Phylogenetic composition and properties of bacteria coexisting with the fungus Hypholoma fasciculare in decaying wood , 2009, The ISME Journal.

[9]  A. Ulrich,et al.  Cellulose-degrading potentials and phylogenetic classification of carboxymethyl-cellulose decomposing bacteria isolated from soil. , 2002, Systematic and applied microbiology.

[10]  T. Cajthaml,et al.  Chemical composition of litter affects the growth and enzyme production by the saprotrophic basidiomycete Hypholoma fasciculare , 2011 .

[11]  I. S. Pretorius,et al.  Microbial Cellulose Utilization: Fundamentals and Biotechnology , 2002, Microbiology and Molecular Biology Reviews.

[12]  D. Zak,et al.  Isolation of Fungal Cellobiohydrolase I Genes from Sporocarps and Forest Soils by PCR , 2008, Applied and Environmental Microbiology.

[13]  R. de Wachter,et al.  Structure of the 16 S ribosomal RNA of the thermophilic cyanobacterium chlorogloeopsis HTF (‘mastigocladus laminosus HTF’) strain PCC7518, and phylogenetic analysis , 1993, FEBS letters.

[14]  Rytas Vilgalys,et al.  Fungal Community Analysis by Large-Scale Sequencing of Environmental Samples , 2005, Applied and Environmental Microbiology.

[15]  R. Knight,et al.  Pyrosequencing-Based Assessment of Soil pH as a Predictor of Soil Bacterial Community Structure at the Continental Scale , 2009, Applied and Environmental Microbiology.

[16]  Adam Godzik,et al.  Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences , 2006, Bioinform..

[17]  M. Kimura,et al.  Bacterial populations assimilating carbon from 13C-labeled plant residue in soil: Analysis by a DNA-SIP approach , 2011 .

[18]  P. Vandamme,et al.  Collimonas arenae sp. nov. and Collimonas pratensis sp. nov., isolated from (semi-)natural grassland soils. , 2008, International journal of systematic and evolutionary microbiology.

[19]  James R. Cole,et al.  The Ribosomal Database Project: improved alignments and new tools for rRNA analysis , 2008, Nucleic Acids Res..

[20]  P. Baldrian,et al.  Degradation of cellulose by basidiomycetous fungi. , 2008, FEMS microbiology reviews.

[21]  H. Drake,et al.  Metabolic responses of novel cellulolytic and saccharolytic agricultural soil Bacteria to oxygen. , 2009, Environmental microbiology.

[22]  Jean-Michel Claverie,et al.  Phylogeny.fr: robust phylogenetic analysis for the non-specialist , 2008, Nucleic Acids Res..

[23]  K. Schleifer,et al.  Phylogenetic identification and in situ detection of individual microbial cells without cultivation. , 1995, Microbiological reviews.

[24]  R. Dick,et al.  Fungal communities, succession, enzymes, and decomposition. , 2002 .

[25]  B. Berg,et al.  Litter Decomposition: a guide to Carbon and Nutrient Turnover , 2006 .

[26]  W. Liesack,et al.  Mucilaginibacter paludis gen. nov., sp. nov. and Mucilaginibacter gracilis sp. nov., pectin-, xylan- and laminarin-degrading members of the family Sphingobacteriaceae from acidic Sphagnum peat bog. , 2007, International journal of systematic and evolutionary microbiology.

[27]  F. Martin,et al.  454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. , 2009, The New phytologist.

[28]  T. Cajthaml,et al.  Transformation of Quercus petraea litter: successive changes in litter chemistry are reflected in differential enzyme activity and changes in the microbial community composition. , 2011, FEMS microbiology ecology.

[29]  Lynne Boddy,et al.  Living in a fungal world: impact of fungi on soil bacterial niche development. , 2005, FEMS microbiology reviews.

[30]  P. Baldrian,et al.  Production of extracellular enzymes and degradation of biopolymers by saprotrophic microfungi from the upper layers of forest soil , 2010, Plant and Soil.

[31]  Yan Sun,et al.  Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP) , 2008, BMC Microbiology.

[32]  Jizhong Zhou,et al.  Biphenyl-utilizing bacteria and their functional genes in a pine root zone contaminated with polychlorinated biphenyls (PCBs) , 2007, The ISME Journal.

[33]  C. Dennis Breakdown of Cellulose by Yeast Species , 1972 .

[34]  M. Vandenbol,et al.  Fungi Unearthed: Transcripts Encoding Lignocellulolytic and Chitinolytic Enzymes in Forest Soil , 2010, PloS one.

[35]  S. Trumbore,et al.  Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. , 2007, The New phytologist.

[36]  T. Bruns,et al.  ITS primers with enhanced specificity for basidiomycetes ‐ application to the identification of mycorrhizae and rusts , 1993, Molecular ecology.

[37]  L. Deacon,et al.  Diversity and function of decomposer fungi from a grassland soil , 2006 .

[38]  J. Kopecký,et al.  Active and total microbial communities in forest soil are largely different and highly stratified during decomposition , 2011, The ISME Journal.

[39]  P. Baldrian Ectomycorrhizal fungi and their enzymes in soils: is there enough evidence for their role as facultative soil saprotrophs? , 2009, Oecologia.

[40]  L. Tedersoo,et al.  454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. , 2010, The New phytologist.

[41]  R. B. Jackson,et al.  Responses of soil cellulolytic fungal communities to elevated atmospheric CO₂ are complex and variable across five ecosystems. , 2011, Environmental microbiology.

[42]  A. Tsuneda,et al.  In vitro decomposition of Sphagnum by some microfungi resembles white rot of wood. , 2006, FEMS microbiology ecology.

[43]  M. D. Aitken,et al.  Multiple DNA Extractions Coupled with Stable-Isotope Probing of Anthracene-Degrading Bacteria in Contaminated Soil , 2011, Applied and Environmental Microbiology.

[44]  W. Achouak,et al.  Identification of cellulolytic bacteria in soil by stable isotope probing. , 2007, Environmental microbiology.

[45]  L. Tranvik,et al.  Interactions of bacteria and fungi on decomposing litter: differential extracellular enzyme activities. , 2006, Ecology.

[46]  T. White Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics , 1990 .

[47]  T. Schmidt,et al.  Influence of Plant Polymers on the Distribution and Cultivation of Bacteria in the Phylum Acidobacteria , 2010, Applied and Environmental Microbiology.

[48]  K. Masaki,et al.  An acidic and thermostable carboxymethyl cellulase from the yeast Cryptococcus sp. S-2: purification, characterization and improvement of its recombinant enzyme production by high cell-density fermentation of Pichia pastoris. , 2008, Protein expression and purification.

[49]  L. Boddy,et al.  Saprotrophic basidiomycete mycelia and their interspecific interactions affect the spatial distribution of extracellular enzymes in soil. , 2011, FEMS microbiology ecology.

[50]  A. Ulrich,et al.  Diversity and Activity of Cellulose-Decomposing Bacteria, Isolated from a Sandy and a Loamy Soil after Long-Term Manure Application , 2008, Microbial Ecology.

[51]  Bernard Henrissat,et al.  Three Genomes from the Phylum Acidobacteria Provide Insight into the Lifestyles of These Microorganisms in Soils , 2009, Applied and Environmental Microbiology.