Soil fertility determines whether ectomycorrhizal fungi accelerate or decelerate decomposition in a temperate forest
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
J 4369
Austrian Science Fund FWF - Austria
P 29087
Austrian Science Fund FWF - Austria
PubMed
37084070
PubMed Central
PMC7614611
DOI
10.1111/nph.18930
Knihovny.cz E-zdroje
- Klíčová slova
- Fagus sylvatica (beech) forest, Gadgil effect, carbon cycle, nitrogen mining, plant-soil feedback, priming, soil fungal communities, tree girdling,
- MeSH
- dusík MeSH
- houby MeSH
- lesy MeSH
- mykorhiza * MeSH
- půda MeSH
- půdní mikrobiologie MeSH
- stromy mikrobiologie MeSH
- uhlík MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- dusík MeSH
- půda MeSH
- uhlík MeSH
Ectomycorrhizal (ECM) fungi can both accelerate and decelerate decomposition of organic matter in forest soils, but a mechanistic understanding of this differential influence is limited. Here, we tested how ECM fungi affect decomposition along a natural fertility gradient in a temperate forest of European beech. Trees were girdled to reduce belowground carbon supply to the soil. Girdling shifted soil fungal community composition and decreased hyphal biomass production and soil CO2 efflux, indicating a reduced ECM fungal activity. Girdling also affected decomposition processes, but the effects depended on fertility. Our results indicate that ECM fungi decelerate decomposition under conditions of low fertility while under conditions of high fertility ECM fungi and their host roots have an accelerating effect. We conclude that both acceleration and deceleration of decomposition of organic matter by ECM fungi can occur within a forest, with soil fertility determining the direction and magnitude of these effects. We suggest a positive feedback between fertility, stand productivity and soil carbon and nitrogen dynamics that is mediated to a large extent by ECM fungi.
Zobrazit více v PubMed
Agerer R. Fungal relationships and structural identity of their ectomycorrhizae. Mycological Progress. 2006;5:67–107.
Anthony MA, Crowther TW, van der Linde S, Suz LM, Bidartondo MI, Cox F, Schaub M, Rautio P, Ferretti M, Vesterdal L. Forest tree growth is linked to mycorrhizal fungal composition and function across Europe. The ISME Journal. 2022;16:1–10. PubMed PMC
Argiroff WA, Zak DR, Pellitier PT, Upchurch RA, Belke JP. Decay by ectomycorrhizal fungi couples soil organic matter to nitrogen availability. Ecology Letters. 2022;25:391–404. PubMed
Averill C, Hawkes CV. Ectomycorrhizal fungi slow soil carbon cycling. Ecology Letters. 2016;19:937–947. PubMed
Bahram M, Vanderpool D, Pent M, Hiltunen M, Ryberg M. The genome and microbiome of a dikaryotic fungus (Inocybe terrigena, Inocybaceae) revealed by metagenomics. Environmental Microbiology Reports. 2018;10:155–166. PubMed
Baldrian P. Ectomycorrhizal fungi and their enzymes in soils: is there enough evidence for their role as facultative soil saprotrophs? Oecologia. 2009;161:657–660. PubMed
Barbaroux C, Bréda N, Dufrêne E. Distribution of above-ground and below-ground carbohydrate reserves in adult trees of two contrasting broad-leaved species (Quercus petraea and Fagus sylvatica) New Phytologist. 2003;157:605–615. PubMed
Barthod J, Dignac MF, Le Mer G, Bottinelli N, Watteau F, Kögel-Knabner I, Rumpel C. How do earthworms affect organic matter decomposition in the presence of clay-sized minerals? Soil Biology and Biochemistry. 2020;143:107730
Bastida F, Garcia C, Fierer N, Eldridge DJ, Bowker MA, Abades S, Alfaro FD, Berhe AA, Cutler NA, Gallardo A. Global ecological predictors of the soil priming effect. Nature Communications. 2019;10:1–9. PubMed PMC
Bödeker ITM, Clemmensen KE, de Boer W, Martin F, Olson Å, Lindahl BD. Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems. New Phytologist. 2014;203:245–256. PubMed
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. PubMed PMC
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 Phytologist. 2015;206:1274–1282. PubMed
Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science. 2013;339:1615–1618. PubMed
Courty P-E, Pritsch K, Schloter M, Hartmann A, Garbaye J. Activity profiling of ectomycorrhiza communities in two forest soils using multiple enzymatic tests. New Phytologist. 2005;167:309–319. PubMed
Djukic I, Kepfer-Rojas S, Schmidt IK, Larsen KS, Beier C, Berg B, Verheyen K. Early stage litter decomposition across biomes. Science of the Total Environment. 2018;628–629:1369–1394. PubMed
Duddigan S, Shaw LJ, Alexander PD, Collins CD. Chemical underpinning of the tea bag index: an examination of the decomposition of tea leaves. Applied and Environmental Soil Science. 2020;2020:6085180
Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–2461. PubMed
Fernandez CW, Kennedy PG. Revisiting the ‘Gadgil effect’: do interguild fungal interactions control carbon cycling in forest soils? New Phytologist. 2016;209:1382–1394. PubMed
Fernandez CW, See CR, Kennedy PG. Decelerated carbon cycling by ectomycorrhizal fungi is controlled by substrate quality and community composition. New Phytologist. 2020;226:569–582. PubMed
Frey SD. Mycorrhizal fungi as mediators of soil organic matter dynamics. Annual Review of Ecology, Evolution, and Systematics. 2019;50:237–259.
Gadgil RL, Gadgil P. Influence of clearfelling on decomposition of Pinus radiata litter. New Zealand Journal of Forest Science. 1978;8:213–224.
Gadgil RL, Gadgil PD. Mycorrhiza and litter decomposition. Nature. 1971;233:133. PubMed
Gadgil RL, Gadgil PD. Suppression of litter decomposition by mycorrhizal roots of Pinus radiata. New Zealand Journal of Forest Science. 1975;5:33–41.
Gorfer M, Mayer M, Berger H, Rewald B, Tallian C, Matthews B, Sanden H, Katzensteiner K, Godbold DL. High fungal diversity but low seasonal dynamics and ectomycorrhizal abundance in a mountain beech forest. Microbial Ecology. 2021;82:243–256. PubMed PMC
Guenet B, Camino-Serrano M, Ciais P, Tifafi M, Maignan F, Soong JL, Janssens IA. Impact of priming on global soil carbon stocks. Global Change Biology. 2018;24:1873–1883. PubMed
Heinemeyer A, Wilkinson M, Vargas R, Subke J-A, Casella E, Morison J, Ineson P. Exploring the “overflow tap” theory: linking forest soil CO2 fluxes and individual mycorrhizosphere components to photosynthesis. Biogeosciences. 2012;9:79–95.
Hobbie EA. Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology. 2006;87:563–569. PubMed
Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Hogberg MN, Nyberg G, Ottosson-Lofvenius M, Read DJ. Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature. 2001;411:789–792. PubMed
Huo C, Luo Y, Cheng W. Rhizosphere priming effect: a meta-analysis. Soil Biology and Biochemistry. 2017;111:78–84.
Jones DL, Nguyen C, Finlay RD. Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant and Soil. 2009;321:5–33.
Jörgensen K, Clemmensen KE, Wallander H, Lindahl BD. Do ectomycorrhizal exploration types reflect mycelial foraging strategies? New Phytologist. 2022;237:576–584. PubMed PMC
Kaiser C, Fuchslueger L, Koranda M, Gorfer M, Stange CF, Kitzler B, Rasche F, Strauss J, Sessitsch A, Zechmeister-Boltenstern S, et al. Plants control the seasonal dynamics of microbial N cycling in a beech forest soil by belowground C allocation. Ecology. 2011;92:1036–1051. PubMed
Keuskamp JA, Dingemans BJJ, Lehtinen T, Sarneel JM, Hefting MM. Tea Bag Index: a novel approach to collect uniform decomposition data across ecosystems. Methods in Ecology and Evolution. 2013;4:1070–1075.
Kobler J, Jandl R, Dirnböck T, Mirtl M, Schindlbacher A. Effects of stand patchiness due to windthrow and bark beetle abatement measures on soil CO2 efflux and net ecosystem productivity of a managed temperate mountain forest. European Journal of Forest Research. 2015;134:683–692.
Kohler A, Kuo A, Nagy LG, Morin E, Barry KW, Buscot F, Canbäck B, Choi C, Cichocki N, Clum A. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nature Genetics. 2015;47:410–415. PubMed
Kyaschenko J, Clemmensen KE, Karltun E, Lindahl BD. Below-ground organic matter accumulation along a boreal forest fertility gradient relates to guild interaction within fungal communities. Ecology Letters. 2017;20:1546–1555. PubMed
Lang AK, Jevon FV, Vietorisz CR, Ayres MP, Hatala MJ. Fine roots and mycorrhizal fungi accelerate leaf litter decomposition in a northern hardwood forest regardless of dominant tree mycorrhizal associations. New Phytologist. 2021;230:316–326. PubMed
Lang F, Bauhus J, Frossard E, George E, Kaiser K, Kaupenjohann M, Krüger J, Matzner E, Polle A, Prietzel J, et al. Phosphorus in forest ecosystems: new insights from an ecosystem nutrition perspective. Journal of Plant Nutrition and Soil Science. 2016;179:129–135.
Lindahl BD, Kyaschenko J, Varenius K, Clemmensen KE, Dahlberg A, Karltun E, Stendahl J. A group of ectomycorrhizal fungi restricts organic matter accumulation in boreal forest. Ecology Letters. 2021;24:1341–1351. PubMed
Lindahl BD, Tunlid A. Ectomycorrhizal fungi–potential organic matter decomposers, yet not saprotrophs. New Phytologist. 2015;205:1443–1447. PubMed
Liu CM, Kachur S, Dwan MG, Abraham AG, Aziz M, Hsueh P-R, Huang Y-T, Busch JD, Lamit LJ, Gehring CA. FungiQuant: a broad-coverage fungal quantitative real-time PCR assay. BMC Microbiology. 2012;12:255. PubMed PMC
Mayer M, Matthews B, Rosinger C, Sandén H, Godbold DL, Katzensteiner K. Tree regeneration retards decomposition in a temperate mountain soil after forest gap disturbance. Soil Biology and Biochemistry. 2017a;115:490–498.
Mayer M, Rewald B, Matthews B, Sanden H, Rosinger C, Katzensteiner K, Gorfer M, Berger H, Tallian C, Berger TW, et al. Soil fertility relates to fungal-mediated decomposition and organic matter turnover in a temperate mountain forest. New Phytologist. 2021;231:777–790. PubMed PMC
Mayer M, Sandén H, Rewald B, Godbold DL, Katzensteiner K. Increase in heterotrophic soil respiration by temperature drives decline in soil organic carbon stocks after forest windthrow in a mountainous ecosystem. Functional Ecology. 2017b;31:1163–1172.
Miranda KM, Espey MG, Wink DA. A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide. 2001;5:62–71. PubMed
Nacke H, Goldmann K, Schöning I, Pfeiffer B, Kaiser K, Castillo-Villamizar GA, Schrumpf M, Buscot F, Daniel R, Wubet T. Fine spatial scale variation of soil microbial communities under European beech and Norway spruce. Frontiers in Microbiology. 2016;7:2067. PubMed PMC
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minichin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. VEGAN: community ecology package. 2016 R package v.2.3-5 [WWW document] URL https://cran.r-project.org/web/packages/vegan/index.html .
Olsson PA, Jakobsen I, Wallander H. Mycorrhizal ecology. Berlin & Heidelberg, Germany: Springer; 2002. Foraging and resource allocation strategies of mycorrhizal fungi in a patchy environment; pp. 93–115.
ÖNORM L 1084. Chemical analyses of soils – determination of carbonate taking into account air pressure and temperature. Vienna, Austria: Austrian Standards Institute; 1999.
Orwin KH, Kirschbaum MU, St John MG, Dickie IA. Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment. Ecology Letters. 2011;14:493–502. PubMed
Pellitier PT, Zak DR. Ectomycorrhizal fungi and the enzymatic liberation of nitrogen from soil organic matter: why evolutionary history matters. New Phytologist. 2018;217:68–73. PubMed
Phillips RP, Brzostek E, Midgley MG. The mycorrhizal-associated nutrient economy: a new framework for predicting carbon–nutrient couplings in temperate forests. New Phytologist. 2013;199:41–51. PubMed
Pinheiro JC, Bates DM, DebRoy S, Sarkar D, R Core Team NLME: linear and nonlinear mixed effects models. 2014. R package v. 3.1-117 [WWW document] URL https://cran.r-project.org/web/packages/nlme/nlme.pdf .
Põlme S, Abarenkov K, Nilsson RH, Lindahl BD, Clemmensen KE, Kauserud H, Nguyen N, Kjøller R, Bates ST, Baldrian P. FUNGALTRAITS: a user-friendly traits database of fungi and fungus-like stramenopiles. Fungal Diversity. 2020;105:1–16.
R Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2021.
Read D, Perez-Moreno J. Mycorrhizas and nutrient cycling in ecosystems – a journey towards relevance? New Phytologist. 2003;157:475–492. PubMed
Reichstein M, Bednorz F, Broll G, Kätterer T. Temperature dependence of carbon mineralisation: conclusions from a long-term incubation of subalpine soil samples. Soil Biology and Biochemistry. 2000;32:947–958.
Rhine E, Mulvaney R, Pratt E, Sims G. Improving the Berthelot reaction for determining ammonium in soil extracts and water. Soil Science Society of America Journal. 1998;62:473–480.
Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584. PubMed PMC
Schindlbacher A, Schnecker J, Takriti M, Borken W, Wanek W. Microbial physiology and soil CO2 efflux after 9 years of soil warming in a temperate forest – no indications for thermal adaptations. Global Change Biology. 2015;21:4265–4277. PubMed PMC
Smith GR, Wan J. Resource-ratio theory predicts mycorrhizal control of litter decomposition. New Phytologist. 2019;223:1595–1606. PubMed
Sterkenburg E, Clemmensen KE, Ekblad A, Finlay RD, Lindahl BD. Contrasting effects of ectomycorrhizal fungi on early and late stage decomposition in a boreal forest. The ISME Journal. 2018;12:2187–2197. PubMed PMC
Subke J-A, Inglima I, Cotrufo FM. Trends and methodological impacts in soil CO2 efflux partitioning: a metaanalytical review. Global Change Biology. 2006;12:921–943.
Tedersoo L, Anslan S, Bahram M, Pölme S, Riit T, Liiv I, Kõljalg U, Kisand V, Nilsson H, Hildebrand F. Shotgun metagenomes and multiple primer pair-barcode combinations of amplicons reveal biases in metabarcoding analyses of fungi. MycoKeys. 2015;10:1–43.
Trevathan-Tackett SM, Kepfer-Rojas S, Engelen AH, York PH, Ola A, Li J, Kelleway JJ, Jinks KI, Jackson EL, Adame MF. Ecosystem type drives tea litter decomposition and associated prokaryotic microbiome communities in freshwater and coastal wetlands at a continental scale. Science of the Total Environment. 2021;782:146819. PubMed
Unterwurzacher V, Pogner C, Berger H, Strauss J, Strauss-Goller S, Gorfer M. Validation of a quantitative PCR based detection system for indoor mold exposure assessment in bioaerosols. Environmental Science: Processes & Impacts. 2018;20:1454–1468. PubMed
Van Der Heijden MG, Martin FM, Selosse MA, Sanders IR. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytologist. 2015;205:1406–1423. PubMed
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. PubMed
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 Phytologist. 2001;151:753–760. PubMed
Wubet T, Christ S, Schöning I, Boch S, Gawlich M, Schnabel B, Fischer M, Buscot F. Differences in soil fungal communities between European beech (Fagus sylvatica L.) dominated forests are related to soil and understory vegetation. PLoS ONE. 2012;7:e47500. PubMed PMC
Zak DR, Pellitier PT, Argiroff W, Castillo B, James TY, Nave LE, Averill C, Beidler KV, Bhatnagar J, Blesh J. Exploring the role of ectomycorrhizal fungi in soil carbon dynamics. New Phytologist. 2019;223:33–39. PubMed
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM. Mixed effects models and extensions in ecology with R. New York, NY, USA: Springer; 2009.
RefSeq
PRJNA521677, PRJNA895381, SAMN12582230%2013SAMN12582341, SAMN31508622%2013SAMN31508877, MK626959%2013MK627467