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Fungal community composition shifts along a leaf degradation gradient in a European beech forest

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Abstract

Aims

The fungal communities in living and decomposed leaves of European Beech (Fagus sylvatica) were compared to identify the phyllosphere fungi involved in litter decomposition at a site in Bavaria, Germany.

Methods

New primers were designed to cover a broad range of fungal ribosomal DNA sequence diversity. Following ‘environmental PCR’, clone libraries from each of five samples of living leaves (surface-sterilized and untreated), freshly fallen, initially and highly decomposed leaves, were screened using RFLP fingerprinting.

Results

Statistical analysis (ANOSIM) revealed that the fungal communities colonizing living (a) and initially decomposed leaves (c) significantly differed between each other and from freshly fallen (b) and highly decomposed leaves (d). Fungal assemblages of a and d were statistically indistinguishable from each other and from the endophyllous fungal community in living leaves.

Conclusions

The results showed that endophyllous fungi play a role throughout the whole decomposition process of beech leaf litter. Therefore, clarification of the life cycle of certain endophytic and/or soil fungi may only be achieved by considering both phyllosphere and soil habitats.

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References

  • Baldrian P, Lindahl B (2011) Decomposition in forest ecosystems: after decades of research still novel findings. Fungal Ecol 4:359–361

    Article  Google Scholar 

  • Baldrian P, Kolařík M, Stursová M, Kopecký J, Valášková V, Větrovský T, Žifčáková L, Šnajdr J, Rídl J, Vlček C, Voříšková J (2011a) Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISME J. doi:10.1038/ismej.2011.95

  • Baldrian P, Voříšková J, Dobiášová P, Merhautová V, Lisá L, Valášková V (2011b) Production of extracellular enzymes and degradation of biopolymers by saprotrophic microfungi from the upper layers of forest soil. Plant Soil 338(1):111–125

    Article  CAS  Google Scholar 

  • Berg B, McClaugherty C (2008) Plant litter: decomposition, humus formation, carbon sequestration. Springer, Berlin, Heidelberg

    Google Scholar 

  • Bills GF, Christensen M, Powell MJ, Thorn G (2004) Saprobic soil fungi. In: Mueller GM, Bills GF, Foster MS (eds) Biodiversity of fungi: inventory and monitoring methods. Elsevier, Boston, pp 271–302

    Google Scholar 

  • Borneman J, Hartin RJ (2000) PCR primers that amplify fungal rRNA genes from environmental samples. Appl Environ Microbiol 66:4356–4360

    Article  PubMed  CAS  Google Scholar 

  • Bridge PD, Spooner BM (2001) Soil fungi: diversity and detection. Plant Soil 232:147–154

    Article  CAS  Google Scholar 

  • Bridge PD, Roberts PJ, Spooner BM, Panchal G (2003) On the unreliability of published DNA sequences. New Phytol 160:43–48

    Article  CAS  Google Scholar 

  • Bringmark E (1989) Spatial variation in soil-pH of beech forests in relation to buffering properties and soil depths. Oikos 54:165–177

    Article  Google Scholar 

  • Brock PM, Döring H, Bidartondo MI (2009) How to know unknown fungi: the role of a herbarium. New Phytol 181:719–724

    Article  PubMed  Google Scholar 

  • Buée M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F (2009) 454 pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449–456

    Article  PubMed  Google Scholar 

  • Câmara MPS, Palm ME, van Berkum P, O’Neill NR (2002) Molecular phylogeny of Leptosphaeria and Phaeosphaeria. Mycologia 94:630–640

    Article  PubMed  Google Scholar 

  • Chapman MG, Underwood AJ (1999) Ecological patterns in multivariate assemblages: information and interpretation of negative values in ANOSIM tests. Mar Ecol Prog Ser 180:257–265

    Article  Google Scholar 

  • Coleman DC, Crossley DA Jr, Hendrix PF (2004) Fundamentals of soil ecology, 2nd edn. Academic, Burlington

    Google Scholar 

  • Collado J, Platas G, Paulus B, Bills GF (2007) High-throughput culturing of fungi from plant litter by a dilution-to-extinction technique. FEMS Microbiol Ecol 60:521–533

    Article  PubMed  CAS  Google Scholar 

  • d’Annunzio R, Zeller B, Nicolas M, Dhôte J-F, Saint-André L (2008) Decomposition of European beech (Fagus sylvatica) litter: combining quality theory and 15N labelling experiments. Soil Biol Biochem 40:322–333

    Article  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. http://www.R-project.org

  • Dickie IA (2010) Insidious effects of sequencing errors on perceived diversity in molecular surveys. New Phytol 188:916–918

    Article  PubMed  Google Scholar 

  • Espinosa-Garcia FJ, Langenheim JH (1990) The endophytic fungal community in leaves of a coastal redwood population – diversity and spatial patterns. New Phytol 116:89–97

    Article  Google Scholar 

  • Flessa F, Kehl A, Kohl M (2010) RFLPtools. R package version 1.0

  • Frankland JC (1998) Fungal succession – unravelling the unpredictable. Mycol Res 102:1–15

    Article  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  PubMed  CAS  Google Scholar 

  • Gewin V (2006) Genomics: discovery in the dirt. Nature 439(7075):384–386

    Article  PubMed  CAS  Google Scholar 

  • Hashizume Y, Fukuda K, Sahashi N (2010) Effects of summer temperature on fungal endophyte assemblages in Japanese beech (Fagus crenata) leaves in pure beech stands. Botany 88:266–274

    Article  CAS  Google Scholar 

  • Heilmann-Clausen J, Christensen M (2003) Fungal diversity on decaying beech logs – implications for sustainable forestry. Biodivers Conserv 12:953–973

    Article  Google Scholar 

  • Jaccard P (1901) Étude comparative de la distribution florale dans une portion des Alpes et des Jura. Bull Soc Vaudoise Sci Nat 37:547–579

    Google Scholar 

  • Johnston P (1998) Leaf endophytes of manuka (Leptospermum scoparium). Mycol Res 102:1009–1016

    Article  Google Scholar 

  • Jumpponen A, Jones KL (2010) Seasonally dynamic fungal communities in the Quercus macrocarpa phyllosphere differ between urban and nonurban environments. New Phytol 186:496–513

    Article  PubMed  CAS  Google Scholar 

  • Kaneko R, Kaneko S (2004) The effect of bagging branches on levels of endophytic fungal infection in Japanese beech leaves. For Pathol 34:65–78

    Article  Google Scholar 

  • Kharwar RN, Gond SK, Kumar A, Mishra A (2010) A comparative study of endophytic and epiphytic fungal association with leaf of Eucalyptus citriodora Hook., and their antimicrobial activity. World J Microbiol Biotech 26:1941–1948

    Article  Google Scholar 

  • Koide K, Osono T, Takeda H (2005) Colonization and lignin decomposition of Camellia japonica leaf litter by endophytic fungi. Mycoscience 46:280–286

    Article  Google Scholar 

  • Korkama-Rajala T, Müller MM, Pennanen T (2008) Decomposition and fungi of needle litter from slow- and fast-growing Norway spruce (Picea abies) clones. Microb Ecol 56:76–89

    Article  PubMed  Google Scholar 

  • Kurtzman CP, Fell JW, Boekhout T (2010) The yeasts, a taxonomic study. Elsevier, New York

    Google Scholar 

  • Lee DW, Collins TM (2001) Phylogenetic and ontogenetic influences on the distribution of anthocyanins and betacyanins in leaves of tropical plants. Int J Plant Sci 162:1141–1153

    Article  CAS  Google Scholar 

  • Liers C, Arnstadt T, Ullrich R, Hofrichter M (2011) Patterns of lignin degradation and oxidative enzyme secretion by different wood- and litter-colonizing basidiomycetes and ascomycetes grown on beech-wood. FEMS Microbiol Ecol 78:91–102

    Article  PubMed  CAS  Google Scholar 

  • Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Hogberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–620

    Article  PubMed  CAS  Google Scholar 

  • Lindeberg G (1946) On the decomposition of lignin and cellulose in litter caused by soil-inhabiting Hymenomycetes. Arkiv Bot 33A:1–10

    Google Scholar 

  • Lorenzi E, Lorando E, Picco AM (2006) Microfunghi endofitici ed epifitici di Picea abies (L.) Karst. in ambiente natural ed antropizzato in Lombardia. Forest 3:426–436

    Article  Google Scholar 

  • Magri D, Vendramin GG, Comps B, Dupanloup I, Geburek T, Gomory D, Latalowa M, Litt T, Paule L, Roure JM, Tantau I, van der Knaap WO, Petit RJ, de Beaulieu JL (2006) A new scenario for the quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol 171:199–221

    Article  PubMed  CAS  Google Scholar 

  • Manter DK, Vivanco JM (2007) Use of the ITS primers, ITS1F and ITS4, to characterize fungal abundance and diversity in mixed-template samples by qPCR and length heterogeneity analysis. J Microbiol Meth 71:7–14

    Article  CAS  Google Scholar 

  • Miyamoto T, Igarashi T, Takahashi K (2000) Lignin-degrading ability of litter-decomposing basidiomycetes from Picea forests of Hokkaido. Mycoscience 41:105–110

    Article  CAS  Google Scholar 

  • Moorhead DL, Sinsabaugh RL (2006) A theoretical model of litter decay and microbial interaction. Ecol Monogr 76:151–174

    Article  Google Scholar 

  • Nagahama T, Hamamoto M, Nakase T, Shimamura S, Horikoshi K (2006) Phylogenetic relationship within the Erythrobasidium clade: molecular phylogenies, secondary structure, and intron positions inferred from partial sequences of ribosomal RNA and elongation factor-1 alpha genes. J Gen Appl Microbiol 52:37–45

    Article  PubMed  CAS  Google Scholar 

  • Osono T (2002) Phyllosphere fungi on leaf litter of Fagus crenata: occurrence, colonization, and succession. Can J Bot 80:460–469

    Article  Google Scholar 

  • Osono T (2006) Role of phyllosphere fungi of forest trees in the development of decomposer fungal communities and decomposition processes of leaf litter. Can J Microbiol 52:701–716

    Article  PubMed  CAS  Google Scholar 

  • Osono T (2008) Endophytic and epiphytic phyllosphere fungi of Camellia japonica: seasonal and leaf age-dependent variations. Mycologia 100:387–391

    Article  PubMed  Google Scholar 

  • Osono T, Takeda H (1999) Decomposing ability of interior and surface fungal colonizers of beech leaves with reference to lignin decomposition. Eur J Soil Biol 35:51–56

    Article  Google Scholar 

  • Osono T, Takeda H (2001) Organic chemical and nutrient dynamics in decomposing beech leaf litter in relation to fungal ingrowth and succession during 3-year decomposition processes in a cool temperate deciduous forest in Japan. Ecol Res 16:649–670

    Article  CAS  Google Scholar 

  • Parrott D, Yang L, Shama L, Fischer AM (2005) Senescence is accelerated, and several proteases are induced by carbon “feast” conditions in barley (Hordeum vulgare L.) leaves. Planta 222:989–1000

    Article  PubMed  CAS  Google Scholar 

  • Peršoh D, Theuerl S, Buscot F, Rambold G (2008) Towards a universally adaptable method for quantitative extraction of high-purity nucleic acids from soil. J Microbiol Meth 75:19–24

    Article  Google Scholar 

  • Peršoh D, Melcher M, Flessa F, Rambold G (2010) First fungal community analyses of endophytic ascomycetes associated with Viscum album ssp. austriacum and its host Pinus sylvestris. Fungal Biol 114:585–596

    Article  PubMed  Google Scholar 

  • Peršoh D, Weig AR, Rambold G (2012) A transcriptome-targeting EcoChip for assessing functional mycodiversity. Microarrays 1:25–41. doi:10.3390/microarrays1010025

    Article  Google Scholar 

  • Polisky B, Greene P, Garfin DE, McCarthy BJ, Goodman HM, Boyer HW (1975) Specificity of substrate recognition by the EcoRI restriction endonuclease. PNAS 72:3310–3314

    Article  PubMed  CAS  Google Scholar 

  • Polz MF, Cavanaugh CM (1998) Bias in template-to-product ratios in multitemplate PCR. Appl Environ Microbiol 64:3724–3730

    PubMed  CAS  Google Scholar 

  • Promputtha I, Lumyong S, Dhanasekaran V, McKenzie EH, Hyde KD, Jeewon R (2007) A phylogenetic evaluation of whether endophytes become saprotrophs at host senescence. Microbial Ecol 53:579–590

    Article  Google Scholar 

  • Prosser JI (2010) Replicate or lie. Environ Microbiol 12:1806–1810

    Article  PubMed  CAS  Google Scholar 

  • Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196

    Article  PubMed  CAS  Google Scholar 

  • Santamaria J, Bayman P (2005) Fungal epiphytes and endophytes of coffee leaves (Coffea arabica). Microbial Ecol 50:1–8

    Article  Google Scholar 

  • Saunders M, Kohn LM (2009) Evidence for alteration of fungal endophyte community assembly by host defense compounds. New Phytol 182:229–238

    Article  PubMed  CAS  Google Scholar 

  • Schubert K, Groenewald JZ, Braun U, Dijksterhuis J, Starink M, Hill CF, Zalar P, de Hoog GS, Crous PW (2007) Biodiversity in the Cladosporium herbarum complex (Davidiellaceae, Capnodiales), with standardisation of methods for Cladosporium taxonomy and diagnostics. Stud Mycol 58:105–156

    Article  PubMed  CAS  Google Scholar 

  • Šnajdr J, Cajthaml T, Valášková V, Merhautová V, Petránková M, Spetz P, Leppänen K, Baldrian P (2011) Transformation of Quercus petraea litter: successive changes in litter chemistry are reflected in differential enzyme activity and changes in the microbial community composition. FEMS Microbiol Ecol 75:291–303

    Article  PubMed  Google Scholar 

  • Staab JF, Balajee SA, Marr KA (2009) Aspergillus section Fumigati typing by PCR-restriction fragment polymorphism. J Clin Microbiol 47:2079–2083

    Article  PubMed  CAS  Google Scholar 

  • Stone JK, Polishook JD, White JF (2004) Endophytic fungi. In: Mueller GM, Bills GF, Foster MS (eds) Biodiversity of fungi: inventory and monitoring methods. Elsevier, Boston, pp 241–270

    Google Scholar 

  • Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fisher MC (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol 31(1):21–32

    Article  PubMed  CAS  Google Scholar 

  • Tedersoo L, Nilsson RH, Abarenkov K, Jairus T, Sadam A, Saar I, Bahram M, Bechem E, Chuyong G, Koljalg U (2010) 454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytol 188:291–301

    Article  PubMed  CAS  Google Scholar 

  • Troedsson T, Tamm CO (1969) Small-scale spatial variation in forest soil properties and its implications for sampling procedures: Variabiliteten i några av skogsmarkens egenskaper inom små ytor och dess betydelse för markprovtagningsmetodiken. In: Flower-Ellis JGK (ed) Studia forestalia Suecica. Skogshögskolan, Faculty of Forest Sciences, Swedish University of Agricultural Sciences, Stockholm

    Google Scholar 

  • Unterseher M (2011) Diversity of fungal endophytes in temperate forest trees. In: Pirttilä AM, Frank AC (eds) Endophytes of forest trees – biology and applications. Springer, Netherlands, pp 31–46

    Chapter  Google Scholar 

  • Unterseher M, Schnittler M (2009) Dilution-to-extinction cultivation of leaf-inhabiting endophytic fungi in beech (Fagus sylvatica L.) – different cultivation techniques influence fungal biodiversity assessment. Mycol Res 113:645–654

    Article  PubMed  Google Scholar 

  • Unterseher M, Reiher A, Finstermeier K, Otto P, Morawetz W (2007) Species richness and distribution patterns of leaf-inhabiting endophytic fungi in a temperate forest canopy. Mycol Prog 6:201–212

    Article  Google Scholar 

  • Unterseher M, Jumpponen A, Opik M, Tedersoo L, Moora M, Dormann CF, Schnittler M (2011) Species abundance distributions and richness estimations in fungal metagenomics – lessons learned from community ecology. Mol Ecol 20:275–285

    Article  PubMed  Google Scholar 

  • van Elsas JD, Garbeva P, Salles J (2002) Effects of agronomical measures on the microbial diversity of soils as related to the suppression of soil-borne plant pathogens. Biodegradation 13:29–40

    Article  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Shinsky J, White T (eds) PCR protocols: a guide to methods and applications. Academic, London, pp 315–322

    Google Scholar 

  • Wildman HG, Parkinson D (1979) Microfungal succession on living leaves of Populus tremuloides. Can J Bot 57:2800–2811

    Article  Google Scholar 

  • Zeier J (2005) Age-dependent variations of local and systemic defence responses in Arabidopsis leaves towards an avirulent strain of Pseudomonas syringae. Physiol Mol Plant Pathol 66:30–39

    Article  CAS  Google Scholar 

  • Žifčáková L, Dobiášová P, Kolářová Z, Koukol O, Baldrian P (2011) Enzyme activities of fungi associated with Picea abies needles. Fungal Ecol 4:427–436

    Article  Google Scholar 

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Acknowledgments

We appreciate the support given by Ulrich Mergner (Ebrach) in allocating the sampling site. Dominik Begerow and Andrey Yurkov (both Bochum) shared with us details on Erythrobasidiaceae. Fabienne Flessa and Alexandra Kehl provided valuable information concerning data analysis, Sebastian Werner and Christina Leistner assisted with laboratory work (all Bayreuth). Suggestions of Marc Stadler (Bayreuth) helped to improve the manuscript.

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Authors and Affiliations

  1. Department of Mycology, University of Bayreuth, Universitätsstraße 30, 95440, Bayreuth, Germany

    Derek Peršoh, Julia Segert, Anja Zigan & Gerhard Rambold

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  1. Derek Peršoh
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  2. Julia Segert
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  3. Anja Zigan
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  4. Gerhard Rambold
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Correspondence to Derek Peršoh.

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Responsible Editor: Duncan D. Cameron.

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Table S1

Details on the assignment to RFLP types, genotypes and taxa of selected sequences. The most similar sequence found in GenBank is given in the following section. The assigned name is listed in the third part, together with the “Bit Score” of the worst matching sequence considered for the name assignment. The sequences considered for name assignment (i.e. sequences obtaining “Bit Scores” which are at least 0.9 times as high as the “Bit Score” obtained by the best matching sequence), are categorized as matches (i.e. sequences deposited under names matching the assigned name), ambiguities (i.e. sequences deposited under names neither confirming nor objecting the assigned name), and the number of outliers (i.e. sequences deposited under names not considered for the name assignment). (XLS 39 kb)

Table S2

Fraction of sequences in selected taxa matched by the primer sequences. The percentage of sequences matched perfectly (0 MM) and with one mismatch (1 MM) by the primers among the checked sequences (N) is given. (DOC 38 kb)

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Peršoh, D., Segert, J., Zigan, A. et al. Fungal community composition shifts along a leaf degradation gradient in a European beech forest. Plant Soil 362, 175–186 (2013). https://doi.org/10.1007/s11104-012-1271-y

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