• This record comes from PubMed

Clearcutting alters decomposition processes and initiates complex restructuring of fungal communities in soil and tree roots

. 2018 Mar ; 12 (3) : 692-703. [epub] 20180115

Language English Country England, Great Britain Media print-electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

Links

PubMed 29335638
PubMed Central PMC5864242
DOI 10.1038/s41396-017-0027-3
PII: 10.1038/s41396-017-0027-3
Knihovny.cz E-resources

Forest management practices often severely affect forest ecosystem functioning. Tree removal by clearcutting is one such practice, producing severe impacts due to the total reduction of primary productivity. Here, we assessed changes to fungal community structure and decomposition activity in the soil, roots and rhizosphere of a Picea abies stand for a 2-year period following clearcutting compared to data from before tree harvest. We found that the termination of photosynthate flow through tree roots into soil is associated with profound changes in soil, both in decomposition processes and fungal community composition. The rhizosphere, representing an active compartment of high enzyme activity and high fungal biomass in the living stand, ceases to exist and starts to resemble bulk soil. Decomposing roots appear to separate from bulk soil and develop into hotspots of decomposition and important fungal biomass pools. We found no support for the involvement of ectomycorrhizal fungi in the decomposition of roots, but we found some evidence that root endophytic fungi may have an important role in the early stages of this process. In soil, activity of extracellular enzymes also decreased in the long term following the end of rhizodeposition by tree roots.

See more in PubMed

Baldrian P. Forest microbiome: diversity, complexity and dynamics. FEMS Microbiol Rev. 2017;41:109–30. PubMed

Litton CM, Raich JW, Ryan MG. Carbon allocation in forest ecosystems. Glob Change Biol. 2007;13:2089–109. doi: 10.1111/j.1365-2486.2007.01420.x. DOI

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;339:1615–8. doi: 10.1126/science.1231923. PubMed DOI

Dijkstra FA, Cheng WX. Interactions between soil and tree roots accelerate long-term soil carbon decomposition. Ecol Lett. 2007;10:1046–53. doi: 10.1111/j.1461-0248.2007.01095.x. PubMed DOI

Kuzyakov Y. Priming effects: interactions between living and dead organic matter. Soil Biol Biochem. 2010;42:1363–71. doi: 10.1016/j.soilbio.2010.04.003. DOI

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;411:789–92. doi: 10.1038/35081058. PubMed DOI

Churchland C, Grayston SJ, Bengtson P. Spatial variability of soil fungal and bacterial abundance: consequences for carbon turnover along a transition from a forested to clearcut site. Soil Biol Biochem. 2013;63:5–13. doi: 10.1016/j.soilbio.2013.03.015. DOI

Štursová M, Šnajdr J, Cajthaml T, Bárta J, Šantrůčková H, Baldrian P. When the forest dies: the response of forest soil fungi to a bark beetle-induced tree dieback. ISME J. 2014;8:1920–31. doi: 10.1038/ismej.2014.37. PubMed DOI PMC

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. doi: 10.1007/s11104-013-1630-3. DOI

Bååth E, Nilsson LO, Göransson H, Wallander H. Can the extent of degradation of soil fungal mycelium during soil incubation be used to estimate ectomycorrhizal biomass in soil? Soil Biol Biochem. 2004;36:2105–9. doi: 10.1016/j.soilbio.2004.06.004. DOI

Wallander H, Göransson H, Rosengren U. Production, standing biomass and natural abundance of 15N and 13C in ectomycorrhizal mycelia collected at different soil depths in two forest types. Oecologia. 2004;139:89–97. doi: 10.1007/s00442-003-1477-z. PubMed DOI

Courty PE, Buéé M, Diedhiou AG, Frey-Klett P, Le Tacon F, Rineau F, et al. The role of ectomycorrhizal communities in forest ecosystem processes: New perspectives and emerging concepts. Soil Biol Biochem. 2010;42:679–98. doi: 10.1016/j.soilbio.2009.12.006. DOI

Baldrian P. Ectomycorrhizal fungi and their enzymes in soils: is there enough evidence for their role as facultative soil saprotrophs? Oecologia. 2009;161:657–60. doi: 10.1007/s00442-009-1433-7. PubMed DOI

Talbot JM, Allison SD, Treseder KK. Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct Ecol. 2008;22:955–63. doi: 10.1111/j.1365-2435.2008.01402.x. DOI

Lindahl BD, Tunlid A. Ectomycorrhizal fungi—potential organic matter decomposers, yet not saprotrophs. New Phytol. 2015;205:1443–7. doi: 10.1111/nph.13201. PubMed DOI

Lindahl BD, de Boer W, Finlay RD. Disruption of root carbon transport into forest humus stimulates fungal opportunists at the expense of mycorrhizal fungi. ISME J. 2010;4:872–81. doi: 10.1038/ismej.2010.19. PubMed DOI

Bödeker ITM, Lindahl BD, Olson A, Clemmensen KE. Mycorrhizal and saprotrophic fungal guilds compete for the same organic substrates but affect decomposition differently. Funct Ecol. 2016;30:1967–78. doi: 10.1111/1365-2435.12677. DOI

Averill C, Hawkes CV. Ectomycorrhizal fungi slow soil carbon cycling. Ecol Lett. 2016;19:937–47. doi: 10.1111/ele.12631. PubMed DOI

Fernandez CW, Kennedy PG. Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? New Phytol. 2016;209:1382–94. doi: 10.1111/nph.13648. PubMed DOI

Gadgil RL, Gadgil PD. Suppression of litter decomposition by mycorrhizal roots of Pinus radiata. New Zeal J Sci. 1975;5:33–41.

Brabcová V, Nováková M, Davidová A, Baldrian P. Dead fungal mycelium in forest soil represents a decomposition hotspot and a habitat for a specific microbial community. New Phytol. 2016;210:1369–81. doi: 10.1111/nph.13849. PubMed DOI

Holden SR, Treseder KK. A meta-analysis of soil microbial biomass responses to forest disturbances. Front Microbiol. 2013;4:163. doi: 10.3389/fmicb.2013.00163. PubMed DOI PMC

Grebenc T, Christensen M, Vilhar U, Cater M, Martin MP, Simoncic P, et al. Response of ectomycorrhizal community structure to gap opening in natural and managed temperate beech-dominated forests. Can J Res. 2009;39:1375–86. doi: 10.1139/X09-072. DOI

Jones MD, Durall DM, Cairney JWG. Ectomycorrhizal fungal communities in young forest stands regenerating after clearcut logging. New Phytol. 2003;157:399–422. doi: 10.1046/j.1469-8137.2003.00698.x. PubMed DOI

Kyaschenko J, Clemmensen KE, Hagenbo A, Karltun E, Lindahl BD. Shift in fungal communities and associated enzyme activities along an age gradient of managed Pinus sylvestris stands. ISME J. 2017;11:863–74. doi: 10.1038/ismej.2016.184. PubMed DOI PMC

Cardenas E, Kranabetter JM, Hope G, Maas KR, Hallam S, Mohn WW. Forest harvesting reduces the soil metagenomic potential for biomass decomposition. ISME J. 2015;9:2465–76. doi: 10.1038/ismej.2015.57. PubMed DOI PMC

Wang GG, Van Lear DH, Hu HF, Kapeluck PR. Accounting carbon storage in decaying root systems of harvested forests. Ambio. 2012;41:284–91. doi: 10.1007/s13280-011-0161-5. PubMed DOI PMC

Lytle DE, Cronan CS. Comparative soil CO2 evolution, litter decay, and root dynamics in clearcut and uncut spruce–fir forest. Ecol Manag. 1998;103:121–8. doi: 10.1016/S0378-1127(97)00182-5. DOI

Langley AJ, Chapman SK, Hungate BA. Ectomycorrhizal colonization slows root decomposition: the post-mortem fungal legacy. Ecol Lett. 2006;9:955–9. doi: 10.1111/j.1461-0248.2006.00948.x. PubMed DOI

Li XF, Lange H. A modified soil coring method for measuring fine root production, mortality and decomposition in forests. Soil Biol Biochem. 2015;91:192–9. doi: 10.1016/j.soilbio.2015.08.015. PubMed DOI

Wallander H, Nilsson LO, Hagerberg D, Bååth E. Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phytol. 2001;151:753–60. doi: 10.1046/j.0028-646x.2001.00199.x. PubMed DOI

Šnajdr J, Valášková V, Merhautová V, Cajthaml T, Baldrian P. Activity and spatial distribution of lignocellulose-degrading enzymes during forest soil colonization by saprotrophic basidiomycetes. Enzym Microb Technol. 2008;43:186–92. doi: 10.1016/j.enzmictec.2007.11.008. DOI

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. doi: 10.1007/s11104-010-0296-3. DOI

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;74:2902–7. doi: 10.1128/AEM.02161-07. PubMed DOI PMC

Ihrmark K, Bodeker ITM, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, et al. New primers to amplify the fungal ITS2 region—evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol Ecol. 2012;82:666–77. doi: 10.1111/j.1574-6941.2012.01437.x. PubMed DOI

Žifčáková L, Větrovský T, Howe A, Baldrian P. Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter. Environ Microbiol. 2016;18:288–301. doi: 10.1111/1462-2920.13026. PubMed DOI

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;49:1027–37. doi: 10.1007/s00374-013-0801-y. DOI

Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996–8. doi: 10.1038/nmeth.2604. PubMed DOI

Koljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, et al. Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol. 2013;22:5271–7. doi: 10.1111/mec.12481. PubMed DOI

Lindahl BD, Nilsson RH, Tedersoo L, Abarenkov K, Carlsen T, Kjøller R, et al. Fungal community analysis by high-throughput sequencing of amplified markers—a user’s guide. New Phytol. 2013;199:288–99. doi: 10.1111/nph.12243. PubMed DOI PMC

Tedersoo L, Bahram M, Polme S, Koljalg U, Yorou NS, Wijesundera R, et al. Global diversity and geography of soil fungi. Science. 2014;346:1256688. doi: 10.1126/science.1256688. PubMed DOI

R Core Development Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2008.

Sariyildiz T. Effects of tree species and topography on fine and small root decomposition rates of three common tree species (Alnus glutinosa, Picea orientalis and Pinus sylvestris) in Turkey. Ecol Manag. 2015;335:71–86. doi: 10.1016/j.foreco.2014.09.030. DOI

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;6:248–58. doi: 10.1038/ismej.2011.95. PubMed DOI PMC

Baldrian P, Zrustova P, Tlaskal V, Davidova A, Merhautova V, Vrska T. Fungi associated with decomposing deadwood in a natural beech-dominated forest. Fungal Ecol. 2016;23:109–22. doi: 10.1016/j.funeco.2016.07.001. DOI

Brzostek ER, Dragoni D, Brown ZA, Phillips RP. Mycorrhizal type determines the magnitude and direction of root-induced changes in decomposition in a temperate forest. New Phytol. 2015;206:1274–82. doi: 10.1111/nph.13303. PubMed DOI

Žifčáková L, Větrovský T, Lombard V, Henrissat B, Howe A, Baldrian P. Feed in summer, rest in winter: Microbial carbon utilization in forest topsoil. Microbiome. 2017;5:122. doi: 10.1186/s40168-017-0340-0. PubMed DOI PMC

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. 2011;75:291–303. doi: 10.1111/j.1574-6941.2010.00999.x. PubMed DOI

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;6:2199–218. doi: 10.1038/ismej.2012.84. PubMed DOI PMC

Kaiser C, Koranda M, Kitzler B, Fuchslueger L, Schnecker J, Schweiger P, et al. Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil. New Phytol. 2010;187:843–58. doi: 10.1111/j.1469-8137.2010.03321.x. PubMed DOI PMC

Pec GJ, Karst J, Taylor DL, Cigan PW, Erbilgin N, Cooke JEK, et al. Change in soil fungal community structure driven by a decline in ectomycorrhizal fungi following a mountain pine beetle (Dendroctonus ponderosae) outbreak. New Phytol. 2017;213:864–73. doi: 10.1111/nph.14195. PubMed DOI

Parker TC, Sadowsky J, Dunleavy H, Subke JA, Frey SD, Wookey PA. Slowed biogeochemical cycling in sub-arctic birch forest linked to reduced mycorrhizal growth and community change after a defoliation event. Ecosystems. 2017;20:316–30. doi: 10.1007/s10021-016-0026-7. PubMed DOI PMC

Hambleton S, Sigler L. Meliniomyces, a new anamorph genus for root-associated fungi with phylogenetic affinities to Rhizoscyphus ericae (Hymenoscyphus ericae), Leotiomycetes. Stud Mycol. 2005;53:1–27. doi: 10.3114/sim.53.1.1. DOI

Kerley SJ, Read DJ. The biology of mycorrhiza in the Ericaceae XX. Plant and mycorrhizal necromass as nitrogenous substrates for the ericoid mycorrhizal fungus Hymenscyphus ericae and its host. New Phytol. 1998;139:353–60. doi: 10.1046/j.1469-8137.1998.00189.x. PubMed DOI

Kohler A, Kuo A, Nagy LG, Morin E, Barry KW, Buscot F, et al. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat Genet. 2015;47:410–5. doi: 10.1038/ng.3223. PubMed DOI

Bending GD, Read DJ. Lignin and soluble phenolic degradation by ectomycorrhizal and ericoid mycorrhizal fungi. Mycol Res. 1997;101:1348–54. doi: 10.1017/S0953756297004140. DOI

Grelet G, Martino E, Dickie IA, Tajuddin R, Artz R. Ecology of ericoid mycorrhizal fungi. Molecular Mycorrhizal Symbiosis. New York: Wiley; 2016. p. 405-19.

Grünig CR, Queloz V, Sieber TN, Holdenrieder O. Dark septate endophytes (DSE) of the Phialocephala fortinii s.l.–Acephala applanata species complex in tree roots: classification, population biology, and ecology. Botany. 2008;86:1355–69. doi: 10.1139/B08-108. DOI

Schlegel M, Munsterktter M, Guldener U, Bruggmann R, Duo A, Hainaut M, et al. Globally distributed root endophyte Phialocephala subalpina links pathogenic and saprophytic lifestyles. BMC Genom. 2016;17:1015. doi: 10.1186/s12864-016-3369-8. PubMed DOI PMC

Voříšková J, Baldrian P. Fungal community on decomposing leaf litter undergoes rapid successional changes. ISME J. 2013;7:477–86. doi: 10.1038/ismej.2012.116. PubMed DOI PMC

Žifčáková L, Dobiášová P, Kolářová Z, Koukol O, Baldrian P. Enzyme activities of fungi associated with Picea abies needles. Fungal Ecol. 2011;4:427–36. doi: 10.1016/j.funeco.2011.04.002. DOI

Parfitt D, Hunt J, Dockrell D, Rogers HJ, Boddy L. Do all trees carry the seeds of their own destruction? PCR reveals numerous wood-decay fungi latently present in sapwood of a wide range of angiosperm trees. Fungal Ecol. 2010;3:338–46. doi: 10.1016/j.funeco.2010.02.001. DOI

Song ZW, Kennedy PG, Liew FJ, Schilling JS. Fungal endophytes as priority colonizers initiating wood decomposition. Funct Ecol. 2017;31:407–18. doi: 10.1111/1365-2435.12735. DOI

Smith GR, Finlay RD, Stenlid J, Vasaitis R, Menkis A. Growing evidence for facultative biotrophy in saprotrophic fungi: data from microcosm tests with 201 species of wood-decay basidiomycetes. New Phytol. 2017;215:747–55. doi: 10.1111/nph.14551. PubMed DOI

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...