Coniferous forests cover extensive areas of the boreal and temperate zones. Owing to their primary production and C storage, they have an important role in the global carbon balance. Forest disturbances such as forest fires, windthrows or insect pest outbreaks have a substantial effect on the functioning of these ecosystems. Recent decades have seen an increase in the areas affected by disturbances in both North America and Europe, with indications that this increase is due to both local human activity and global climate change. Here we examine the structural and functional response of the litter and soil microbial community in a Picea abies forest to tree dieback following an invasion of the bark beetle Ips typographus, with a specific focus on the fungal community. The insect-induced disturbance rapidly and profoundly changed vegetation and nutrient availability by killing spruce trees so that the readily available root exudates were replaced by more recalcitrant, polymeric plant biomass components. Owing to the dramatic decrease in photosynthesis, the rate of decomposition processes in the ecosystem decreased as soon as the one-time litter input had been processed. The fungal community showed profound changes, including a decrease in biomass (2.5-fold in the litter and 12-fold in the soil) together with the disappearance of fungi symbiotic with tree roots and a relative increase in saprotrophic taxa. Within the latter group, successive changes reflected the changing availability of needle litter and woody debris. Bacterial biomass appeared to be either unaffected or increased after the disturbance, resulting in a substantial increase in the bacterial/fungal biomass ratio.

Faculty of Science University of South Bohemia České Budějovice Czech Republic

Institute of Microbiology of the ASCR v v i Vídeňská 1083 Praha 4 Czech Republic

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Adams HD, Macalady AK, Breshears DD, Allen CD, Stephenson NL, Saleska SR, Huxman TE, McDowell Ng. Climate-induced tree mortality: Earth system consequences. Eos, Trans Amer Geophys Union. 2010;91:153–154.

Baldrian P, Kolařík M, Štursová M, Kopecký J, Valášková V, Větrovský T, et al. Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISME J. 2012;6:248–258. PubMed PMC

Baldrian P, Větrovský T, Cajthaml T, Dobiášová P, Petránková M, Šnajdr J, et al. Estimation of fungal biomass in forest litter and soil. Fungal Ecol. 2013;6:1–11.

Bače R, Svoboda M, Pouska V, Janda P, Červenka J. Natural regeneration in Central-European subalpine spruce forests: which logs are suitable for seedling recruitment. Forest Ecol Manag. 2012;266:254–262.

Bouget C, Duelli P. The effects of windthrow on forest insect communities: a literature review. Biol Conserv. 2004;118:281–299.

Bradshaw CJ, Warkentin IG, Sodhi NS. Urgent preservation of boreal carbon stocks and biodiversity. Trends Ecol Evol. 2009;24:541–548. PubMed

Breshears DD, Myers OB, Meyer CW, Barnes FJ, Zou CB, Allen CD, et al. Tree die-off in response to global change-type drought: mortality insights from a decade of plant water potential measurements. Front Ecol Environ. 2009;7:185–189.

Brunner I, Bakker MR, Bjork RG, Hirano Y, Lukac M, Aranda X, et al. Fine-root turnover rates of European forests revisited: an analysis of data from sequential coring and ingrowth cores. Plant Soil. 2013;362:357–372.

Bárta J, Applová M, Vaněk D, Krištůfková M, Šantrůčková H. Effect of available P and phenolics on mineral N release in acidified spruce forest: connection with lignin-degrading enzymes and bacterial and fungal communities. Biogeochemistry. 2010;97:71–87.

Bååth E, Anderson TH. Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem. 2003;35:955–963.

Bödeker ITM, Nygren CMR, Taylor AFS, Olson A, Lindahl BD. ClassII peroxidase-encoding genes are present in a phylogenetically wide range of ectomycorrhizal fungi. ISME J. 2009;3:1387–1395. PubMed

Chapin FS, III, Matson PA, Vitousek P. Principles of Terrestrial Ecosystem Ecology. Springer Verlag: New York; 2012.

Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, et al. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science. 2013;339:1615–1618. PubMed

Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–2461. PubMed

Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27:2194–2200. PubMed PMC

Ekberg A, Buchmann N, Gleixner G. Rhizospheric influence on soil respiration and decomposition in a temperate Norway spruce stand. Soil Biol Biochem. 2007;39:2103–2110.

Ekblad A, Wallander H, Godbold DL, Cruz C, Johnson D, Baldrian P, et al. The production and turnover of extramatrical mycelium of ectomycorrhizal fungi in forest soils: role in carbon cycling. Plant Soil. 2013;366:1–27.

Giesler R, Högberg MN, Strobel BW, Richter A, Nordgren A, Högberg P. Production of dissolved organic carbon and low-molecular weight organic acids in soil solution driven by recent tree photosynthate. Biogeochemistry. 2007;84:1–12.

Hartmann M, Howes CG, VanInsberghe D, Yu H, Bachar D, Christen R, et al. Significant and persistent impact of timber harvesting on soil microbial communities in Northern coniferous forests. ISME J. 2012;6:2199–2218. PubMed PMC

Hicke JA, Allen CD, Desai AR, Dietze MC, Hall RJ, Ted Hogg EH, et al. Effects of biotic disturbances on forest carbon cycling in the United States and Canada. Global Change Biol. 2012;18:7–34.

Högberg MN, Högberg P. Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytol. 2002;154:791–795. PubMed

Högberg MN, Högberg P, Myrold DD. Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three. Oecologia. 2007;150:590–601. PubMed

Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, et al. Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature. 2001;411:789–792. PubMed

Jonášová M, Prach K. Central-European mountain spruce (Picea abies (L.) Karst.) forests: regeneration of tree species after a bark beetle outbreak. Ecol Eng. 2004;23:15–27.

Jonášová M, Prach K. The influence of bark beetles outbreak vs. salvage logging on ground layer vegetation in Central European mountain spruce forests. Biol Conserv. 2008;141:1525–1535.

Kaňa J, Tahovská K, Kopáček J. Response of soil chemistry to forest dieback after bark beetle infestation. Biogeochemistry. 2013;113:369–383.

Kluber LA, Smith JE, Myrold DD. Distinctive fungal and bacterial communities are associated with mats formed by ectomycorrhizal fungi. Soil Biol Biochem. 2011;43:1042–1050.

Kopáček J, Cudlín P, Svoboda M, Chmelíková E, Kaňa J, Picek T. Composition of Norway spruce litter and foliage in atmospherically acidified and nitrogen-saturated Bohemian Forest stands, Czech Republic. Boreal Environ Res. 2010;15:413–426.

Kopáček J, Kaňa J, Šantrůčková H, Porcal P, Hejzlar J, Picek T, et al. Physical, chemical, and biochemical characteristics of soils in watersheds of the Bohemian Forest lakes: I. Plešné Lake. Silva Gabreta. 2002;8:43–62.

Kurz WA, Dymond CC, Stinson G, Rampley GJ, Neilson ET, Carroll AL, et al. Mountain pine beetle and forest carbon feedback to climate change. Nature. 2008;452:987–990. PubMed

Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, et al. Defining the core Arabidopsis thaliana root microbiome. Nature. 2012;488:86–90. PubMed PMC

Moore DJP, Trahan NA, Wilkes P, Quaife T, Stephens BB, Elder K, et al. Persistent reduced ecosystem respiration after insect disturbance in high elevation forests. Ecol Lett. 2013;16:731–737. PubMed PMC

Myneni RB, Dong J, Tucker CJ, Kaufmann RK, Kauppi PE, Liski J, et al. A large carbon sink in the woody biomass of Northern forests. Proc Natl Acad Sci USA. 2001;98:14784–14789. PubMed PMC

Okland B, Bjornstad ON. A resource-depletion model of forest insect outbreaks. Ecology. 2006;87:283–290. PubMed

Reeder J, Knight R. Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods. 2010;7:668–669. PubMed PMC

Reininger V, Grunig CR, Sieber TN. Host species and strain combination determine growth reduction of spruce and birch seedlings colonized by root-associated dark septate endophytes. Environ Microbiol. 2012;14:1064–1076. PubMed

Ruckstuhl KE, Johnson EA, Miyanishi K. Introduction. The boreal forest and global change. Phil Trans Royal Soc London Ser B. 2008;363:2245–2249. PubMed PMC

Sagova-Mareckova M, Cermak L, Novotna J, Plhackova K, Forstova J, Kopecky J. Innovative methods for soil DNA purification tested in soils with widely differing characteristics. Appl Environ Microbiol. 2008;74:2902–2907. PubMed PMC

Schelhaas MJ, Nabuurs GJ, Schuck A. Natural disturbances in the European forests in the 19th and 20th centuries. Global Change Biol. 2003;9:1620–1633.

Seidl R, Schelhaas MJ, Lexer MJ. Unraveling the drivers of intensifying forest disturbance regimes in Europe. Global Change Biol. 2011;17:2842–2852.

Soja AJ, Tchebakova NM, French NHF, Flannigan MD, Shugart HH, Stocks BJ, et al. Climate-induced boreal forest change: predictions versus current observations. Glob Planet Change. 2007;56:274–296.

Svoboda M, Janda P, Nagel TA, Fraver S, Rejzek J, Bace R. Disturbance history of an old-growth sub-alpine Picea abies stand in the Bohemian Forest, Czech Republic. J Veg Sci. 2012;23:86–97.

Tedersoo L, Nilsson RH, Abarenkov K, Jairus T, Sadam A, Saar I, et al. 454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytol. 2010;188:291–301. PubMed

Tejesvi MV, Sauvola T, Pirttila AM, Ruotsalainen AL. Neighboring Deschampsia flexuosa and Trientalis europaea harbor contrasting root fungal endophytic communities. Mycorrhiza. 2013;23:1–10. PubMed

Tellenbach C, Grunig CR, Sieber TN. Negative effects on survival and performance of Norway spruce seedlings colonized by dark septate root endophytes are primarily isolate-dependent. Environ Microbiol. 2011;13:2508–2517. PubMed

Vacek J, Krejčí F.2009Forest Ecosystems in the Bohemian Forest National Park (in Czech). Lesnická práce: Kostelec nad Černými Lesy, Czech Republic, pp 512.

Voříšková J, Brabcová V, Cajthaml T, Baldrian P. Seasonal dynamics of fungal communities in a temperate forest soil. New Phytol. 2014;201:269–278. PubMed

Větrovský T, Baldrian P. Analysis of soil fungal communities by amplicon pyrosequencing: current approaches to data analysis and the introduction of the pipeline SEED. Biol Fertil Soils. 2013;49:1027–1037.

Waldrop MP, Zak DR. Response of oxidative enzyme activities to nitrogen deposition affects soil concentrations of dissolved organic carbon. Ecosystems. 2006;9:921–933.

Wallander H, Johansson U, Sterkenburg E, Brandström Durling M, Lindahl BD. Production of ectomycorrhizal mycelium peaks during canopy closure in Norway spruce forests. New Phytol. 2010;187:1124–1134. PubMed

White TJ, Bruns T, Lee S, Taylor J.1990Amplification and direct sequencing of fungal ribosomal RNA genes for phylogeneticsIn: Innins MA, Gelfand DH, Sninsky JJ, White TJ (eds)PCR Protocols Academic Press: San Diego, CA; 315–322.

Yarwood SA, Myrold DD, Högberg MN. Termination of belowground C allocation by trees alters soil fungal and bacterial communities in a boreal forest. FEMS Microbiol Ecol. 2009;70:151–162. PubMed

Zeller B, Liu J, Buchmann N, Richter A. Tree girdling increases soil N mineralisation in two spruce stands. Soil Biol Biochem. 2008;40:1155–1166.

Šantrůčková H, Krištůfková M, Vaněk D. Decomposition rate and nutrient release from plant litter of Norway spruce forest in the Bohemian Forest. Biologia. 2006;61:S499–S508.

Šnajdr J, Cajthaml T, Valášková V, Merhautová V, Petránková M, Spetz P, 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. FEMS Microbiol Ecol. 2011a;75:291–303. PubMed

Šnajdr J, Dobiášová P, Větrovský T, Valášková V, Alawi A, Boddy L, et al. Saprotrophic basidiomycete mycelia and their interspecific interactions affect the spatial distribution of extracellular enzymes in soil. FEMS Microbiol Ecol. 2011b;78:80–90. PubMed

Šnajdr J, Valášková V, Merhautová V, Herinková J, Cajthaml T, Baldrian P. Spatial variability of enzyme activities and microbial biomass in the upper layers of Quercus petraea forest soil. Soil Biol Biochem. 2008;40:2068–2075.

Štursová M, Baldrian P. Effects of soil properties and management on the activity of soil organic matter transforming enzymes and the quantification of soil-bound and free activity. Plant Soil. 2011;338:99–110.

Štursová M, Žifčáková L, Leigh MB, Burgess R, Baldrian P. Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers. FEMS Microbiol Ecol. 2012;80:735–746. PubMed

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

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