Abstract
Ectomycorrhizal (ECM) fungi, as symbionts of many tree species in temperate forests, are thought to play an important role in forest regeneration processes after large disturbances. Their reaction to different disturbance and management regimes was studied in spruce forests (Lariceto-Piceetum) 10 years after a severe windthrow in the Tatra National Park (Slovak Republic). ECM community structure was compared between different “management types″—cleared area (EXT), area affected by wildfire (FIRE), uncleared area left for natural development (NEX), and mature forest as a control (REF). Based on Illumina sequencing of soil samples, we determined that the percentage of sequences assigned to ECM fungi decreased with increasing disturbance and management intensity (REF → NEX → EXT → FIRE). Similarly, the total number of ECM species per each of ten sampling points per plot (100 ha) differed between managed (EXT-11 species, FIRE-9) and unmanaged (NEX-16, REF-14) treatments. On the other hand, the percentage of sequences belonging to ericoid mycorrhizal fungi increased. Management type significantly influenced the composition of the ECM community, while vegetation and soil characteristics explained less data variation. The ECM species assemblage of the unmanaged site (NEX) was the most similar to the mature forest, while that of the burnt site was the most different. Thelephora terrestris dominated in all treatments affected by windthrow, accompanied by Tylospora fibrillosa (NEX) and Tylospora asterophora (EXT and FIRE). Management regime was also the most important factor affecting ECM species composition on the roots of spruce seedlings assessed by Sanger sequencing.
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Abarenkov K, Henrik Nilsson R, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AF, Tedersoo L, Ursing BM, Vrålstad T, Liimatainen K, Peintner U, Kõljalg U (2010) The UNITE database for molecular identification of fungi – recent updates and future perspectives. New Phytol 186(2):281–285. https://doi.org/10.1111/j.1469-8137.2009.03160.x
Agerer R (2006) Fungal relationships and structural identity of their ectomycorrhizae. Mycol Prog 5(2):67–107. https://doi.org/10.1007/s11557-006-0505-x
Agerer R, Rambold G (2004-2015) DEEMY - an information system for characterization and determination of ectomycorrhizae. http://www.deemy.de/. Accessed 9 Apr 2015
Barker JS, Simard SW, Jones MD, Durall DM (2013) Ectomycorrhizal fungal community assembly on regenerating Douglas-fir after wildfire and clearcut harvesting. Oecologia 172(4):1179–1189. https://doi.org/10.1007/s00442-012-2562-y
Bernicchia A, Gorjón SP (2010) Corticiaceae s.l. Fungi Europei n°12. Ed. Candusso. Alassio. 1008 p
Bengtsson J, Nilsson SG, Franc A, Menozzi P (2000) Biodiversity, disturbances, ecosystem function and management of European forests. Forest Ecol Manag 132(1):39–50. https://doi.org/10.1016/S0378-1127(00)00378-9
Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2007) GenBank. Nucleic Acids Res 41:36–41
Buscardo E, Rodríguez-Echeverría S, Freitas H, De Angelis P, Pereira JS, Muller LA (2015) Contrasting soil fungal communities in Mediterranean pine forests subjected to different wildfire frequencies. Fungal Divers 70(1):85–99. https://doi.org/10.1007/s13225-014-0294-5
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña 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 Methods 7(5):335–336. https://doi.org/10.1038/nmeth.f.303
Don A, Bärwolff M, Kalbitz K, Andruschkewitsch R, Jungkunst HF, Schulze ED (2012) No rapid soil carbon loss after a windthrow event in the high Tatra. For Ecol Manag 276:239–246. https://doi.org/10.1016/j.foreco.2012.04.010
Dvořák D, Vašutová M, Hofmeister J, Beran M, Hošek J, Běťák J, Burel J, Deckerová H (2017) Macrofungal diversity patterns in central European forests affirm the key importance of old-growth forests. Fungal Ecol 27:145–154. https://doi.org/10.1016/j.funeco.2016.12.003
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996e998
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Fleischer P (2008) Windfall research and monitoring in the high Tatra Mts, objectives, principles, methods and current status. Contrib Geophys Geodesy 38(3):233–248
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts. Mol Ecol 2(2):113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
Glassman SI, Levine CR, DiRocco AM, Battles JJ, Bruns TD (2016) Ectomycorrhizal fungal spore bank recovery after a severe forest fire: some like it hot. ISME J 10(5):1228–1239. https://doi.org/10.1038/ismej.2015.182
Gömöryová E, Střelcová K, Fleischer P, Gömöry D (2011) Soil microbial characteristics at the monitoring plots on windthrow areas of the Tatra National Park (Slovakia): their assessment as environmental indicators. Environ Monit Assess 174(1):31–45. https://doi.org/10.1007/s10661-010-1755-2
Hartmann M, Niklaus PA, Zimmermann S, Schmutz S, Kremer J, Abarenkov K, Lüscher P, Widmer F, Frey B (2014) Resistance and resilience of the forest soil microbiome to logging-associated compaction. ISME J 8(1):226–244
Hußlein M, Kiener H, Křenová Z, Šolar M (2009) EUROPE’S WILD HEART, conference report January 2009, Srní, Czech Republic, ISBN: 3-930977-33-8
Jones MD, Durall DM, Cairney JW (2003) Ectomycorrhizal fungal communities in young forest stands regenerating after clearcut logging. New Phytol 157(3):399–422. https://doi.org/10.1046/j.1469-8137.2003.00698.x
Nicholson BA, Jones MD (2017) Early-successional ectomycorrhizal fungi effectively support extracellular enzyme activities and seedling nitrogen accumulation in mature forests. Mycorrhiza 27(3):247–260. https://doi.org/10.1007/s00572-016-0747-7
Kataja-aho S, Pennanen T, Lensu A, Haimi J (2012) Does stump removal affect early growth and mycorrhizal infection of spruce (Picea Abies) seedlings in clear-cuts? Scand J For Res 27(8):746–753
Katoh K, Asimenos G, Toh H (2009) Multiple alignment of DNA sequences with MAFFT. Methods Mol Biol 537:39–64. https://doi.org/10.1007/978-1-59745-251-9_3
Knudsen H, Vesterholt J (2012) Funga Nordica. Agaricoid, boletoid, calavarioid, cyphelloid and gastroid genera. Nordsvamp, Copenhagen. 1083 p
Kohler A, Kuo A, Nagy LG, Morin E, Barry KW, Buscot F et al (2015) Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat Genet 47(4):410–415. https://doi.org/10.1038/ng.3223
Kõljalg U (1995) Tomentella (Basidiomycota) and related genera in temperate Eurasia. Synopsis Fungorum 9, Fungiflora, Oslo. 213 p
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948. https://doi.org/10.1093/bioinformatics/btm404
Lindahl BD, Nilsson RH, Tedersoo L, Abarenkov K, Carlsen T, Kjøller R, Kõljalg U, Pennanen T, Rosendahl S, Stenlid J, Kauserud H (2013) Fungal community analysis by high-throughput sequencing of amplified markers-a user ‘s guide. New Phytol 199(1):288–299. https://doi.org/10.1111/nph.12243
Mariotte P (2014) Do subordinate species punch above their weight? Evidence from above-and below-ground. New Phytol 203(1):16–21. https://doi.org/10.1111/nph.12789
Menkis A, Uotila A, Arhipova N, Vasaitis R (2010) Effects of stump and slash removal on growth and mycorrhization of Picea Abies seedlings outplanted on a forest clear-cut. Mycorrhiza 20(7):505–509. https://doi.org/10.1007/s00572-010-0299-1
Michalová Z, Morrissey RC, Wohlgemuth T, Bače R, Fleischer P, Svoboda M (2017) Salvage-logging after windstorm leads to structural and functional homogenization of understory layer and delayed spruce tree recovery in Tatra Mts., Slovakia. Forests 8(3):88. https://doi.org/10.3390/f8030088
Nguyen NH, Smith D, Peay K, Kennedy P (2015) Parsing ecological signal from noise in next generation amplicon sequencing. New Phytol 205(4):1389–1393. https://doi.org/10.1111/nph.12923
Nikolcheva LG, Bärlocher F (2004) Taxon-specific fungal primers reveal unexpectedly high diversity during leaf decomposition in a stream. Mycol Prog 3(1):41–49. https://doi.org/10.1007/s11557-006-0075-y
Pickles BJ, Pither J (2014) Still scratching the surface: how much of the “black box” of soil ectomycorrhizal communities remains in the dark? New Phytol 201(4):1101–1105. https://doi.org/10.1111/nph.12616
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. URL https://www.R-project.org/
Rincón A, Santamaría BP, Ocaña L, Verdú M (2014) Structure and phylogenetic diversity of post-fire ectomycorrhizal communities of maritime pine. Mycorrhiza 24(2):131–141. https://doi.org/10.1007/s00572-013-0520-0
Seidl R, Schelhass MJ, Lexer MJ (2011) Unraveling the drivers of intensifying forest disturbance regimes in Europe. Glob Chang Biol 17(9):2842–2852. https://doi.org/10.1111/j.1365-2486.2011.02452.x
Smith AJ, Potvin LR, Lilleskov EA (2015) Fertility-dependent effects of ectomycorrhizal fungal communities on white spruce seedling nutrition. Mycorrhiza 25(8):649–662. https://doi.org/10.1007/s00572-015-0640-9
Spake R, van der Linde S, Newton AC, Suz LM, Bidartondo MI, Doncaster CP (2016) Similar biodiversity of ectomycorrhizal fungi in set-aside plantations and ancient old-growth broadleaved forests. Biol Conserv 194:71–79. https://doi.org/10.1016/j.biocon.2015.12.003
Štursová M, Šnajdr J, Cajthaml T, Bárta J, Šantrůčková H, Baldrian P (2014) When the forest dies: the response of forest soil fungi to a bark beetle-induced tree dieback. ISME I 8(9):1920–1931. https://doi.org/10.1038/ismej.2014.37
Taylor AFS (2002) Fungal diversity in ectomycorrhizal communities: sampling effort and species detection. Plant Soil 244(1/2):19–28. https://doi.org/10.1023/A:1020279815472
Taudière A, Richard F, Carcaillet C (2017) Review on fire effects on ectomycorrhizal symbiosis, an unachieved work for a scalding topic. Forest Ecol Manag 391:446–457. https://doi.org/10.1016/j.foreco.2017.02.043
Tedersoo L, Bahram M, Toots M, Diedhiou AG, Henkel TW, Kjøller R, Morris MH, Nara K, Nouhra E, Peay KG, Põlme S, Ryberg M, Smith ME, Kõljalg U (2012) Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Mol Ecol 21(17):4160–4170. https://doi.org/10.1111/j.1365-294X.2012.05602.x
Tedersoo L, Smith ME (2013) Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biol Rev 27(3-4):83–99. https://doi.org/10.1016/j.fbr.2013.09.001
Ter Braak CJF, Šmilauer P (2012) Canoco reference manual and user’s guide: software for ordination (version 5.0). Microcomputer power, Ithaca, NY, USA
Vašutová M, Edwards-Jonášová M, Baldrian P, Čermák M, Cudlín P (2017) Distinct environmental variables drive the community composition of mycorrhizal and saprotrophic fungi at the alpine treeline ecotone. Fungal Ecol 27:116–124. https://doi.org/10.1016/j.funeco.2016.08.010
Větrovský T, Baldrian P (2013) Analysis of soil fungal communities by amplicon pyrosequencing: current approaches to data analysis and the introduction of the pipeline SEED. Biol Fert Soils 49(8):1027–1037. https://doi.org/10.1007/s00374-013-0801-y
Visser S, Parkinson D (1999) Wildfire vs. clearcutting: impacts on ectomycorrhizal and decomposer fungi. In: Meurisse RT, Ypsilantis WG, Seybold C (Eds.), Proceedings, Pacific northwest forest and rangeland soil organism symposium; 1998 March 17-19; Corvallis, Portland. USDA Forest Service, Pacific northwest Research Station, general technical report PNW-GTR-461, pp. 114–123
Vohník M, Mrnka L, Lukešová T, Bruzone MC, Kohout P, Fehrer J (2013) The cultivable endophytic community of Norway spruce ectomycorrhizas from microhabitats lacking ericaceous hosts is dominated by ericoid mycorrhizal Meliniomyces variabilis. Fungal Ecol 6(4):281–292. https://doi.org/10.1016/j.funeco.2013.03.006
Walker JKM, Ward V, Paterson C, Jones MD (2012) Coarse woody debris retention in subalpine clearcuts affects ectomycorrhizal root tip community structure within fifteen years of harvest. Appl Soil Ecol 60:5–15. https://doi.org/10.1016/j.apsoil.2012.02.017
Walker JK, Ward V, Jones MD (2016) Ectomycorrhizal fungal exoenzyme activity differs on spruce seedlings planted in forests versus clearcuts. Trees 30(2):497–508. https://doi.org/10.1007/s00468-015-1239-7
Wermelinger B (2004) Ecology and management of the spruce bark beetle Ips typographus — a review of recent research. Forest Ecol. Manag. 202(1):67–82. https://doi.org/10.1016/j.foreco.2004.07.018
White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, (eds) PCR Protocols: a guide to methods and applications, San Diego: Academic Press, p. 315–322
Yamamoto K, Degawa Y, Hirose D, Fukuda M, Yamada A (2015) Morphology and phylogeny of four Endogone species and Sphaerocreas pubescens collected in Japan. Mycol Prog 14(10):86. https://doi.org/10.1007/s11557-015-1111-6
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, 574 p. https://doi.org/10.1007/978-0-387-87458-6
Acknowledgements
This work was supported by the Ministry of Education, Youth and Sports of CR within the National Sustainability Program I, grant No. LO1415 and grant No. LD 15044. We thank Filip Holub, Jan Purkyt, Martin Čermák, Ondřej Cudlín, Jan Červenka, and students from the Faculty of Forestry, Mendel University in Brno for field and lab assistance. Petra Havlíčková helped with the amplicon sequencing.
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Vašutová, M., Edwards-Jonášová, M., Veselá, P. et al. Management regime is the most important factor influencing ectomycorrhizal species community in Norway spruce forests after windthrow. Mycorrhiza 28, 221–233 (2018). https://doi.org/10.1007/s00572-018-0820-5
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DOI: https://doi.org/10.1007/s00572-018-0820-5