Abstract
Saprotrophic and ectomycorrhizal (EcM) forest fungi decompose organic matter and mobilize nutrients for host plants, respectively. Competition between the two guilds may cause the so-called Gadgil effect, i.e., decreased litter decomposition rates resulting in increased carbon storage in soil. The Gadgil effect was supposed to even affect global climate, highlighting the necessity to understand fungal distribution and interactions in soil. Searching for evidence of competition between saprotrophic and mycorrhizal fungi, we analyzed the distribution of fungi along a well-stratified vertical spruce forest soil profile in two seasons, i.e., autumn and the following spring. The different soil strata (i.e., two mineral horizons and two organic layers) underneath the litter layer were colonized by distinct fungal communities, which included roughly consistent proportions of all fungal guilds and phyla at each time. However, the community composition changed quantitatively between the sampling dates. Along the vertical soil profile, it differed mostly between the organic layers and the mineral soil, which is supposed to be due to differences in the predominant energy sources (i.e., aboveground litter and rhizodeposition, respectively). Network analyses revealed co-occurrences (i.e., positive correlations of individual abundances) to outweigh mutual exclusions (i.e., negative correlations) between individual fungi in each soil stratum and season. This also applied for interactions between saprotrophic and EcM fungi. Network analyses therefore provided no indications for a possible Gadgil effect. However, considering individual nutrient use efficiencies might refine insights from network analyses in future studies and facilitate linking community dynamics to ecosystem processes.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11557-018-1405-6/MediaObjects/11557_2018_1405_Fig1_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11557-018-1405-6/MediaObjects/11557_2018_1405_Fig2_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11557-018-1405-6/MediaObjects/11557_2018_1405_Fig3_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11557-018-1405-6/MediaObjects/11557_2018_1405_Fig4_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11557-018-1405-6/MediaObjects/11557_2018_1405_Fig5_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11557-018-1405-6/MediaObjects/11557_2018_1405_Fig6_HTML.gif)
Similar content being viewed by others
References
Agerer R (2006) Fungal relationships and structural identity of their ectomycorrhizae. Mycol Progress 5:67–107. https://doi.org/10.1007/s11557-006-0505-x
Anderson IC, Genney DR, Alexander IJ (2014) Fine-scale diversity and distribution of ectomycorrhizal fungal mycelium in a Scots pine forest. New Phytol 201:1423–1430. https://doi.org/10.1111/nph.12637
Averill C, Hawkes CV (2016) Ectomycorrhizal fungi slow soil carbon cycling. Ecol Lett 19:937–947. https://doi.org/10.1111/ele.12631
Averill C, Turner BL, Finzi AC (2014) Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505:543–545. https://doi.org/10.1038/nature12901
Bahram M, Peay KG, Tedersoo L (2015) Local-scale biogeography and spatiotemporal variability in communities of mycorrhizal fungi. New Phytol 205:1454–1463. https://doi.org/10.1111/nph.13206
Baldrian P (2008) Enzymes of saprotrophic basidiomycetes. In: Boddy L, Frankland JC, van West P (eds) British Mycological Society Symposia Series : Ecology of Saprotrophic Basidiomycetes, Volume 28. Academic Press, pp 19–41
Baldrian P, Kolařík M, Štursová M, Kopecký J, Valášková V, Větrovský T, Zifčáková L, Šnajdr J, Rídl J, Vlček C, Voříšková J (2012) Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISME J. 6:248–258. https://doi.org/10.1038/ismej.2011.95
Bálint M, Bahram M, Eren AM, Faust K, Fuhrman JA, Lindahl B, O’Hara RB, Öpik M, Sogin ML, Unterseher M, Tedersoo L (2016) Millions of reads, thousands of taxa. Microbial community structure and associations analyzed via marker genes. FEMS Microbiol Rev 40:686–700. https://doi.org/10.1093/femsre/fuw017
Berg B, McClaugherty C (2014) Plant Litter. Decomposition, humus formation, carbon sequestration, 3rd edn. Springer Berlin, Heidelberg
Berg B, Staaf H (1980) Decomposition rate and chemical changes of scots pine needle litter. II. Influence of chemical composition. Ecol Bull 373–390
Boddy L, Frankland JC, van West P (2008) Ecology of saprotrophic basidiomycetes. British Mycological Society symposium series, vol 28. Elsevier Academic Press, Amsterdam, London
Bödeker ITM, Lindahl BD, Olson Å, Clemmensen KE (2016) Mycorrhizal and saprotrophic fungal guilds compete for the same organic substrates but affect decomposition differently. Funct Ecol doi:https://doi.org/10.1111/1365-2435.12677
Borken W, Kossmann G, Matzner E (2007) Biomass, morphology and nutrient contents of fine roots in four Norway spruce stands. Plant Soil 292:79–93. https://doi.org/10.1007/s11104-007-9204-x
Braakhekke MC, Wutzler T, Beer C, Kattge J, Schrumpf M, Ahrens B, Schöning I, Hoosbeek MR, Kruijt B, Kabat P, Reichstein M (2013) Modeling the vertical soil organic matter profile using Bayesian parameter estimation. Biogeosciences 10:399–420. https://doi.org/10.5194/bg-10-399-2013
Bradford MA, Wieder WR, Bonan GB, Fierer N, Raymond PA, Crowther TW (2016) Managing uncertainty in soil carbon feedbacks to climate change. Nat Clim Change 6:751–758
Bredemeier M, Blanck K, Dohrenbusch A, Lamersdorf N, Meyer AC, Murach D, Parth A, Xu Y-J (1998) The Solling roof project—site characteristics, experiments and results. For Ecol Manag 101:281–293. https://doi.org/10.1016/S0378-1127(97)00143-6
Cairney JWG, Meharg AA (2002) Interactions between ectomycorrhizal fungi and soil saprotrophs. Implications for decomposition of organic matter in soils and degradation of organic pollutants in the rhizosphere. Can J Bot 80:803–809. https://doi.org/10.1139/b02-072
Cannon PF, Kirk PM (2007) Fungal families of the world. CABI, Wallingford
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Meth. 7:335–336. https://doi.org/10.1038/nmeth.f.303
Carreiro MM, Koske RE (1992) Room temperature isolations can bias against selection of low temperature microfungi in temperate forest soils. Mycologia 84:886. https://doi.org/10.2307/3760287
Courty P-E, Franc A, Pierrat J-C, Garbaye J (2008) Temporal changes in the ectomycorrhizal community in two soil horizons of a temperate oak forest. Appl Environ Microbiol 74:5792–5801. https://doi.org/10.1128/AEM.01592-08
Dickie IA, Xu B, Koide RT (2002) Vertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T-RFLP analysis. New Phytol 156:527–535. https://doi.org/10.1046/j.1469-8137.2002.00535.x
Dighton J (2007) Nutrient cycling by saprotrophic fungi in terrestrial habitats. In: Kubicek CP, Druzhinina IS (eds) Environmental and microbial relationships, vol 4. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 287–300
Dix NJ, Webster J (1995) Fungal Ecology. Springer Netherlands, Dordrecht
Dörr N, Kaiser K, Mikutta R, Guggenberger G (2010) Slow response of soil organic matter to the reduction in atmospheric nitrogen deposition in a Norway spruce forest. Glob Chang Biol 16. https://doi.org/10.1111/j.1365-2486.2009.02148.x
Enowashu E, Poll C, Lamersdorf N, Kandeler E (2009) Microbial biomass and enzyme activities under reduced nitrogen deposition in a spruce forest soil. Appl Soil Ecol 43:11–21. https://doi.org/10.1016/j.apsoil.2009.05.003
FAO (1998) World reference base for soil resources. World soil resources reports, 0532-0488, vol 84. Food and Agriculture Organization of the United Nations, Rome
Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J, Huttenhower C (2012) Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol 8:e1002606. https://doi.org/10.1371/journal.pcbi.1002606
Faust K, Lima-Mendez G, Lerat J-S, Sathirapongsasuti JF, Knight R, Huttenhower C, Lenaerts T, Raes J (2015) Cross-biome comparison of microbial association networks. Front Microbiol 6:1200. https://doi.org/10.3389/fmicb.2015.01200
Fernandez CW, Kennedy PG (2016) Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? New Phytol 209:1382–1394. https://doi.org/10.1111/nph.13648
Frankland JC (1998) Fungal succession—unravelling the unpredictable. Mycol Res 102:1–15
Gadgil RL, Gadgil PD (1971) Mycorrhiza and litter decomposition. Nature 233:133. https://doi.org/10.1038/233133a0
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. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
Geyer KM, Kyker-Snowman E, Grandy AS, Frey SD (2016) Microbial carbon use efficiency. Accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter. Biogeochemistry 127:173–188. https://doi.org/10.1007/s10533-016-0191-y
Gougoulias C, Clark JM, Shaw LJ (2014) The role of soil microbes in the global carbon cycle: tracking the below-ground microbial processing of plant-derived carbon for manipulating carbon dynamics in agricultural systems. J Sci Food Agric 94:2362–2371. https://doi.org/10.1002/jsfa.6577
Guerreiro MA, Brachmann A, Begerow D, Peršoh D (2017) Transient leaf endophytes are the most active fungi in 1-year-old beech leaf litter. Fungal Divers 89:237–251. https://doi.org/10.1007/s13225-017-0390-4
Havranek WM, Tranquillini W (1995) Physiological processes during winter dormancy and their ecological significance. In: Smith WK, Roy J, Hinckley TM (eds) Ecophysiology of coniferous forests. Elsevier, pp 95–124
Hudson HJ (1968) The ecology of fungi on plant remains above the soil. New Phytol 67:837–874. https://doi.org/10.1111/j.1469-8137.1968.tb06399.x
Jayasiri SC, Hyde KD, Ariyawansa HA, Bhat J, Buyck B, Cai L, Dai Y-C, Abd-Elsalam KA, Ertz D, Hidayat I, Jeewon R, Jones EBG, Bahkali AH, Karunarathna SC, Liu J-K, Luangsa-ard JJ, Lumbsch HT, Maharachchikumbura SSN, McKenzie EHC, Moncalvo J-M, Ghobad-Nejhad M, Nilsson H, Pang K-L, Pereira OL, Phillips AJL, Raspé O, Rollins AW, Romero AI, Etayo J, Selçuk F, Stephenson SL, Suetrong S, Taylor JE, Tsui CKM, Vizzini A, Abdel-Wahab MA, Wen T-C, Boonmee S, Dai DQ, Daranagama DA, Dissanayake AJ, Ekanayaka AH, Fryar SC, Hongsanan S, Jayawardena RS, Li W-J, Perera RH, Phookamsak R, de Silva NI, Thambugala KM, Tian Q, Wijayawardene NN, Zhao R-L, Zhao Q, Kang J-C, Promputtha I (2015) The Faces of Fungi database. Fungal names linked with morphology, phylogeny and human impacts. Fungal Divers 74:3–18. https://doi.org/10.1007/s13225-015-0351-8
Johansson M-B, Kögel I, Zech W (1986) Changes in the lignin fraction of spruce and pine needle litter during decomposition as studied by some chemical methods. Soil Biol Biochem 18:611–619. https://doi.org/10.1016/0038-0717(86)90084-2
Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere. Carbon trading at the soil–root interface. Plant Soil 321:5–33. https://doi.org/10.1007/s11104-009-9925-0
Kandeler E, Brune T, Enowashu E, Dörr N, Guggenberger G, Lamersdorf N, Philippot L (2009) Response of total and nitrate-dissimilating bacteria to reduced N deposition in a spruce forest soil profile. FEMS Microbiol Ecol 67:444–454. https://doi.org/10.1111/j.1574-6941.2008.00632.x
Keiluweit M, Nico P, Harmon ME, Mao J, Pett-Ridge J, Kleber M (2015) Long-term litter decomposition controlled by manganese redox cycling. Proc Natl Acad Sci U S A 112:60. https://doi.org/10.1073/pnas.1508945112
Kendrick WB (1962) Biological aspects of the decay of Pinus sylvestris leaf litter. Nova Hedwigia 4:313–342
Kirk PM, Cannon PF, Minter DW, Stalpers JA, Ainsworth GC, Bisby GR (2011) Ainsworth & Bisby’s dictionary of the fungi / by P.M. Kirk … [et al.] ; with the assistance of T.V. Andrianova [et al.], 10th ed. CABI Publishing, Wallingford
Kögel-Knabner I (2016) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Fourteen years on Soil Biol Biochem https://doi.org/10.1016/j.soilbio.2016.08.011
Kohler A, Kuo A, Nagy LG, Morin E, Barry KW, Buscot F, Canback B, Choi C, Cichocki N, Clum A, Colpaert J, Copeland A, Costa MD, Dore J, Floudas D, Gay G, Girlanda M, Henrissat B, Herrmann S, Hess J, Hogberg N, Johansson T, Khouja H-R, Labutti K, Lahrmann U, Levasseur A, Lindquist EA, Lipzen A, Marmeisse R, Martino E, Murat C, Ngan CY, Nehls U, Plett JM, Pringle A, Ohm RA, Perotto S, Peter M, Riley R, Rineau F, Ruytinx J, Salamov A, Shah F, Sun H, Tarkka M, Tritt A, Veneault-Fourrey C, Zuccaro A, Tunlid A, Grigoriev IV, Hibbett DS, Martin F (2015) Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat Genet 47:410–415. https://doi.org/10.1038/ng.3223
Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiss M, Larsson K-H (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277. https://doi.org/10.1111/mec.12481
Kramer C, Trumbore S, Fröberg M, Cisneros Dozal LM, Zhang D, Xu X, Santos GM, Hanson PJ (2010) Recent (<4 year old) leaf litter is not a major source of microbial carbon in a temperate forest mineral soil. Soil Biol Biochem 42:1028–1037. https://doi.org/10.1016/j.soilbio.2010.02.021
Kuramae EE, Hillekens RHE, de Hollander M, van der Heijden MGA, van den Berg M, van Straalen NM, Kreyling J (2013) Structural and functional variation in soil fungal communities associated with litter bags containing maize leaf. FEMS Microbiol Ecol 84:519–531. https://doi.org/10.1111/1574-6941.12080
Lashermes G, Gainvors-Claisse A, Recous S, Bertrand I (2016) Enzymatic strategies and carbon use efficiency of a litter-decomposing fungus grown on maize leaves, stems, and roots. Front Microbiol 7:1315. https://doi.org/10.3389/fmicb.2016.01315
Latter PM, Heal OW (1971) A preliminary study of the growth of fungi and bacteria from temperate and Antarctic soils in relation to temperature. Soil Biol Biochem 3:365–379. https://doi.org/10.1016/0038-0717(71)90047-2
Leppälammi-Kujansuu J, Aro L, Salemaa M, Hansson K, Kleja DB, Helmisaari H-S (2014) Fine root longevity and carbon input into soil from below- and aboveground litter in climatically contrasting forests. For Ecol Manag 326:79–90. https://doi.org/10.1016/j.foreco.2014.03.039
Li W, Fu L, Niu B, Wu S, Wooley J (2012) Ultrafast clustering algorithms for metagenomic sequence analysis. Brief Bioinform 13:656–668. https://doi.org/10.1093/bib/bbs035
Lindahl BD, Tunlid A (2015) Ectomycorrhizal fungi—potential organic matter decomposers, yet not saprotrophs. New Phytol 205:1443–1447. https://doi.org/10.1111/nph.13201
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. https://doi.org/10.1111/j.1469-8137.2006.01936.x
Lundberg DS, Yourstone S, Mieczkowski P, Jones CD, Dangl JL (2013) Practical innovations for high-throughput amplicon sequencing. Nat Meth. 10:999–1002. https://doi.org/10.1038/nmeth.2634
Lundell TK, Mäkelä MR, Hildén K (2010) Lignin-modifying enzymes in filamentous basidiomycetes—ecological, functional and phylogenetic review. J Basic Microbiol 50:5–20. https://doi.org/10.1002/jobm.200900338
Mainiero R, Kazda M, Schmid I (2010) Fine root dynamics in 60-year-old stands of Fagus sylvatica and Picea abies growing on haplic luvisol soil. Eur J Forest Res 129:1001–1009. https://doi.org/10.1007/s10342-010-0383-2
Miyamoto T, Igarashi T, Takahashi K (2000) Lignin-degrading ability of litter-decomposing basidiomycetes from Picea forests of Hokkaido. Mycoscience 41:105–110. https://doi.org/10.1007/BF02464317
Moore JAM, Jiang J, Post WM, Classen AT (2015) Decomposition by ectomycorrhizal fungi alters soil carbon storage in a simulation model. Ecosphere 6:art29. https://doi.org/10.1890/ES14-00301.1
Moorhead DL, Sinsabaugh RL (2006) A theoretical model of litter decay and microbial interaction. Ecol Monogr 76:151–174
Mooshammer M, Wanek W, Hammerle I, Fuchslueger L, Hofhansl F, Knoltsch A, Schnecker J, Takriti M, Watzka M, Wild B, Keiblinger KM, Zechmeister-Boltenstern S, Richter A (2014) Adjustment of microbial nitrogen use efficiency to carbon:nitrogen imbalances regulates soil nitrogen cycling. Nat Commun 5:3694. https://doi.org/10.1038/ncomms4694
Mujic AB, Durall DM, Spatafora JW, Kennedy PG (2016) Competitive avoidance not edaphic specialization drives vertical niche partitioning among sister species of ectomycorrhizal fungi. New Phytol 209:1174–1183. https://doi.org/10.1111/nph.13677
Nagy LG, Riley R, Tritt A, Adam C, Daum C, Floudas D, Sun H, Yadav JS, Pangilinan J, Larsson K-H, Matsuura K, Barry K, Labutti K, Kuo R, Ohm RA, Bhattacharya SS, Shirouzu T, Yoshinaga Y, Martin FM, Grigoriev IV, Hibbett DS (2016) Comparative genomics of early-diverging mushroom-forming fungi provides insights into the origins of lignocellulose decay capabilities. Mol Biol Evol 33:959–970. doi:https://doi.org/10.1093/molbev/msv337
Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild. An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248. https://doi.org/10.1016/j.funeco.2015.06.006
O’Brien HE, Parrent JL, Jackson JA, Moncalvo J-M, Vilgalys R (2005) Fungal community analysis by large-scale sequencing of environmental samples. Appl Environ Microbiol 71:5544–5550. https://doi.org/10.1128/AEM.71.9.5544-5550.2005
Ota M, Nagai H, Koarashi J (2013) Root and dissolved organic carbon controls on subsurface soil carbon dynamics. A model approach. J Geophys Res Biogeosci 118:1646–1659. https://doi.org/10.1002/2013JG002379
Peršoh D (2013) Factors sha** community structure of endophytic fungi—evidence from the Pinus-Viscum-system. Fungal Divers 60:55–69. https://doi.org/10.1007/s13225-013-0225-x
Peršoh D (2015) Plant-associated fungal communities in the light of meta’omics. Fungal Divers 75:1–25. https://doi.org/10.1007/s13225-015-0334-9
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 Methods 75:19–24. https://doi.org/10.1016/j.mimet.2008.04.009
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. https://doi.org/10.1016/j.funbio.2010.04.009
Peršoh D, Segert J, Zigan A, Rambold G (2013) Fungal community composition shifts along a leaf degradation gradient in a European beech forest. Plant Soil 362:175–186. https://doi.org/10.1007/s11104-012-1271-y
Persson HÅ, Stadenberg I (2010) Fine root dynamics in a Norway spruce forest (Picea abies (L.) Karst) in eastern Sweden. Plant Soil 330:329–344. https://doi.org/10.1007/s11104-009-0206-8
Poland JA, Brown PJ, Sorrells ME, Jannink J-L (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genoty**-by-sequencing approach. PLoS One 7:e32253. https://doi.org/10.1371/journal.pone.0032253
Ponge J-F (2005) Fungal communities: relation to resource succession. In: Dighton J, White JF, Oudemans P (eds) The fungal community. Its organization and role in the ecosystem, 3rd ed. Taylor & Francis, Boca Raton, FL
Qu L, Makoto K, Choi DS, Quoreshi AM, Koike T (2010) The role of ectomycorrhiza in boreal forest ecosystem. In: Osawa A, Zyryanova OA, Matsuura Y, Kajimoto T, Wein RW (eds) Permafrost ecosystems, vol 209. Springer Netherlands, Dordrecht, pp 413–425
Röhl O, Graupner N, Peršoh D, Kemler M, Mittelbach M, Boenigk J, Begerow D (2017a) Flooding duration affects the structure of terrestrial and aquatic microbial eukaryotic communities. Microb Ecol https://doi.org/10.1007/s00248-017-1085-9
Röhl O, Peršoh D, Mittelbach M, Elbrecht V, Brachmann A, Nuy J, Boenigk J, Leese F, Begerow D (2017b) Distinct sensitivity of fungal freshwater guilds to water quality. Mycol Progress 16:155–169. https://doi.org/10.1007/s11557-016-1261-1
Rosling A, Landeweert R, Lindahl BD, Larsson K-H, Kuyper TW, Taylor AFS, Finlay RD (2003) Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. New Phytol 159:775–783. https://doi.org/10.1046/j.1469-8137.2003.00829.x
Schmidt SK, Wilson KL, Meyer AF, Gebauer MM, King AJ (2008) Phylogeny and ecophysiology of opportunistic “snow molds” from a subalpine forest ecosystem. Microb Ecol 56:681–687. https://doi.org/10.1007/s00248-008-9387-6
Schneider CA, Rasband WS, Eliceiri KW (2012a) NIH Image to ImageJ. 25 years of image analysis. Nat Meth 9:671–675. https://doi.org/10.1038/nmeth.2089
Schneider T, Keiblinger KM, Schmid E, Sterflinger-Gleixner K, Ellersdorfer G, Roschitzki B, Richter A, Eberl L, Zechmeister-Boltenstern S, Riedel K (2012b) Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions. ISME J. 6:1749–1762. https://doi.org/10.1038/ismej.2012.11;
Smith SE, Read D (2008) Mycorrhizal Symbiosis, 3rd edn. Academic Press, London
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. https://doi.org/10.1111/j.1574-6941.2010.00999.x
Spielvogel S, Prietzel J, Leide J, Riedel M, Zemke J, Kögel-Knabner I (2014) Distribution of cutin and suberin biomarkers under forest trees with different root systems. Plant Soil 381:95–110. https://doi.org/10.1007/s11104-014-2103-z
Swift MJ, Heal OW, Anderson JM (1979) Decomposition in terrestrial ecosystems, vol 5. Univ of California Press
Taylor DL, Hollingsworth TN, McFarland JW, Lennon NJ, Nusbaum C, Ruess RW (2014) A first comprehensive census of fungi in soil reveals both hyperdiversity and fine-scale niche partitioning. Ecol Monogr 84:3–20. https://doi.org/10.1890/12-1693.1
Tedersoo L, Bahram M, Polme S, Koljalg U, Yorou NS, Wijesundera R, Villarreal Ruiz L, Vasco-Palacios AM, Thu PQ, Suija A, Smith ME, Sharp C, Saluveer E, Saitta A, Rosas M, Riit T, Ratkowsky D, Pritsch K, Poldmaa K, Piepenbring M, Phosri C, Peterson M, Parts K, Partel K, Otsing E, Nouhra E, Njouonkou AL, Nilsson RH, Morgado LN, Mayor J, May TW, Majuakim L, Lodge DJ, Lee SS, Larsson K-H, Kohout P, Hosaka K, Hiiesalu I, Henkel TW, Harend H, L-d G, Greslebin A, Grelet G, Geml J, Gates G, Dunstan W, Dunk C, Drenkhan R, Dearnaley J, de KA, Dang T, Chen X, Buegger F, Brearley FQ, Bonito G, Anslan S, Abell S, Abarenkov K (2014) Fungal biogeography. Global diversity and geography of soil fungi. Science 1256688:346. https://doi.org/10.1126/science.1256688
Theuerl S, Dörr N, Guggenberger G, Langer U, Kaiser K, Lamersdorf N, Buscot F (2010) Response of recalcitrant soil substances to reduced N deposition in a spruce forest soil: integrating laccase-encoding genes and lignin decomposition. FEMS Microbiol Ecol 73:166–177. https://doi.org/10.1111/j.1574-6941.2010.00877.x
Thevenot M, Dignac M-F, Rumpel C (2010) Fate of lignins in soils. A review. Soil Biol Biochem 42:1200–1211. https://doi.org/10.1016/j.soilbio.2010.03.017
Tibbett M, Cairney JWG (2007) The cooler side of mycorrhizas. Their occurrence and functioning at low temperatures. Can J Bot 85:51–62. https://doi.org/10.1139/b06-152
Timling I, Taylor DL (2012) Peeking through a frosty window. Molecular insights into the ecology of Arctic soil fungi. Fungal Ecol 5:419–429. https://doi.org/10.1016/j.funeco.2012.01.009
Tunlid A, Floudas D, Koide R, Rineau F (2016) Soil organic matter decomposition mechanisms in ectomycorrhizal fungi. In: Martin F (ed) Molecular mycorrhizal symbiosis. John Wiley & Sons, Inc, pp 257–275
Voříšková J, Baldrian P (2012) Fungal community on decomposing leaf litter undergoes rapid successional changes. ISME J 7:477–486. https://doi.org/10.1038/ismej.2012.116
Voříšková J, Brabcová V, Cajthaml T, Baldrian P (2013) Seasonal dynamics of fungal communities in a temperate oak forest soil. New Phytol 201:269–278. https://doi.org/10.1111/nph.12481
Vries Wd, Leeters EEJM (2001) Chemical composition of the humus layer, mineral soil and soil solution of 150 forest stands in the Netherlands in 1990. Alterra-rapport, vol 424.1. Alterra, Green World Research, Wageningen
Weete JD, Gandhi SR (1999) Sterols and fatty acids of the Mortierellaceae. Taxonomic implications. Mycologia 91:642. https://doi.org/10.2307/3761250
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Shinsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Elsevier, pp 315–322
Yurkov A, Wehde T, Kahl T, Begerow D (2012a) Aboveground deadwood deposition supports development of soil yeasts. Diversity 4:453–474. https://doi.org/10.3390/d4040453
Yurkov AM, Kemler M, Begerow D (2012b) Assessment of yeast diversity in soils under different management regimes. Fungal Ecol 5:24–35. https://doi.org/10.1016/j.funeco.2011.07.004
Yurkov AM, Röhl O, Pontes A, Carvalho C, Maldonado C, Sampaio JP (2016a) Local climatic conditions constrain soil yeast diversity patterns in Mediterranean forests, woodlands and scrub biome. FEMS Yeast Res 16:fov103. https://doi.org/10.1093/femsyr/fov103
Yurkov AM, Wehde T, Federici J, Schäfer AM, Ebinghaus M, Lotze-Engelhard S, Mittelbach M, Prior R, Richter C, Röhl O, Begerow D (2016b) Yeast diversity and species recovery rates from beech forest soils. Mycol Progress 15:845–859. https://doi.org/10.1007/s11557-016-1206-8
Zelezniak A, Andrejev S, Ponomarova O, Mende DR, Bork P, Patil KR (2015) Metabolic dependencies drive species co-occurrence in diverse microbial communities. Proc Natl Acad Sci U S A 112:6449–6454. https://doi.org/10.1073/pnas.1421834112
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. https://doi.org/10.1016/j.funeco.2011.04.002
Žifčáková L, Větrovský T, Howe A, Baldrian P (2016) Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter. Environ Microbiol 18:288–301. https://doi.org/10.1111/1462-2920.13026
Acknowledgements
We thank Dirk Böttger and Norbert Lamersdorf (both Göttingen) and our project partners (i.e., working groups of François Buscot, Halle; Georg Guggenberger, Hannover; Barbara Reinhold-Hurek, Bremen; Ellen Kandeler, Hohenheim) for help during the soil sampling and the good cooperation. Christopher Sadlowski (Bochum) supported the library preparation and Andrey Yurkov (Braunschweig) revised the molecular identification of the basidiomycetous yeasts.
The study was designed by DB, DP and GR. DP and GR performed the sampling. NS extracted the DNA and conducted preliminary analyses. AB and DP prepared the amplicon libraries. AB performed the sequencing. DP analyzed the data and wrote the manuscript. All authors discussed and contributed to the final version of the manuscript.
Funding
The project was partly funded by the Deutsche Forschungsgemeinschaft (DFG-project RA 731/9-1).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing interests.
Additional information
Section Editor: Marc Stadler
Rights and permissions
About this article
Cite this article
Peršoh, D., Stolle, N., Brachmann, A. et al. Fungal guilds are evenly distributed along a vertical spruce forest soil profile while individual fungi show pronounced niche partitioning. Mycol Progress 17, 925–939 (2018). https://doi.org/10.1007/s11557-018-1405-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11557-018-1405-6