Abstract
Many trees depend on symbiotic ectomycorrhizal fungi for nutrients in exchange for photosynthetically derived carbohydrates. Trees growing in peatlands, which cover 3% of the earth’s terrestrial surface area yet hold approximately one-third of organic soil carbon stocks, may benefit from ectomycorrhizal fungi that can efficiently forage for nutrients and degrade organic matter using oxidative enzymes such as class II peroxidases. However, such traits may place a higher carbon cost on both the fungi and host tree. To investigate these trade-offs that might structure peatland ectomycorrhizal fungal communities, we sampled black spruce (Picea mariana (Mill.)) seedlings along 100-year-old peatland drainage gradients in Minnesota, USA, that had resulted in higher soil nitrogen and canopy density. Structural equation models revealed that the relative abundance of the dominant ectomycorrhizal fungal genus, Cortinarius, which is known for relatively high fungal biomass coupled with elevated class II peroxidase potential, was negatively linked to site fertility but more positively affected by recent host stem radial growth, suggesting carbon limitation. In contrast, Cenococcum, known for comparatively lower fungal biomass and less class II peroxidase potential, was negatively linked to host stem radial growth and unrelated to site fertility. Like Cortinarius, the estimated relative abundance of class II peroxidase genes in the ectomycorrhizal community was more related to host stem radial growth than site fertility. Our findings indicate a trade-off between symbiont foraging traits and associated carbon costs that consequently structure seedling ectomycorrhizal fungal communities in peatlands.
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References
Agerer R (2001) Exploration types of ectomycorrhizae: a proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114. https://doi.org/10.1007/s005720100108
Albornoz FE, Teste FP, Lambers H et al (2016) Changes in ectomycorrhizal fungal community composition and declining diversity along a 2-million-year soil chronosequence. Mol Ecol 25:4919–4929. https://doi.org/10.1111/mec.13778
Aronesty E (2011) ea-utils: command-line tools for processing biological sequencing data. https://github.com/ExpressionAnalysis/ea-utils. Accessed 3 Mar 2020
Babst F, Alexander MR, Szejner P, Bouriaund O, Klesse S, Roden J, Ciais P, Pouler B, Frank D, Moore DJP, Trouet V (2014) A tree-ring perspective on the terrestrial carbon cycle. Oecologia 176:307–322. https://doi.org/10.1007/s00442-014-3031-6
Bahram M, Põlme S, Kõljalg U, Tedersoo L (2011) A single European aspen (Populus tremula) tree individual may potentially harbour dozens of Cenococcum geophilum ITS genotypes and hundreds of species of ectomycorrhizal fungi. FEMS Microbiol Ecol 75:313–320. https://doi.org/10.1111/j.1574-6941.2010.01000.x
Bergman I, Lundberg P, Nilsson M (1999) Microbial carbon mineralisation in an acid surface peat: effects of environmental factors in laboratory incubations. Soil Biol Biochem 31:1867–1877. https://doi.org/10.1016/S0038-0717(99)00117-0
Bödeker ITM, Clemmensen KE, de Boer W et al (2014) Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems. New Phytol 203:245–256. https://doi.org/10.1111/nph.12791
Bödeker ITM, Nygren CMR, Taylor AFS et al (2009) ClassII peroxidase-encoding genes are present in a phylogenetically wide range of ectomycorrhizal fungi. ISME J 3:1387–1395. https://doi.org/10.1038/ismej.2009.77
Bolyen E, Rideout JR, Dillon MR et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9
Branco S, Bladeiux P, Ellison C, Kuo A, Labutti K, Lipzen A, Grigoriev I, Liao H-L, Vilgalys R, Peay K, Taylor JW, Bruns T (2015) Genetic isolation between two recently diverged populations of a symbiotic fungus. Mol Ecol 24:2747–2758. https://doi.org/10.1111/mec.13132
Bruns TD (1995) Thoughts on the processes that maintain local species diversity of ectomycorrhizal fungi. Plant Soil 170:63–73. https://doi.org/10.1007/BF02183055
Callahan BJ, McMurdie PJ, Rosen MJ et al (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869
Chen DM, Taylor AFS, Burke RM, Cairney JWG (2001) Identification of genes for lignin peroxidases and manganese peroxidases in ectomycorrhizal fungi. New Phytol 152:151–158. https://doi.org/10.1046/j.0028-646X.2001.00232.x
Clemmensen KE, Finlay RD, Dahlberg A, Stenlid J, Wardle DA, Lindahl BD (2015) Carbon sequestration is related to mycorrhizal community shifts during long-term succession in boreal forests. New Phytol 205:1525–1536. https://doi.org/10.1111/nph.13208
Defrenne CE, Philpott TJ, Guichon SHA et al (2019) Shifts in ectomycorrhizal fungal communities and exploration types relate to the environment and fine-root traits across interior Douglas-fir forests of western Canada. Front Plant Sci 10:1–16. https://doi.org/10.3389/fpls.2019.00643
Delgado-Baquerizo M, Reich PB, Khachane AN et al (2017) It is elemental: soil nutrient stoichiometry drives bacterial diversity. Environ Microbiol 19:1176–1188. https://doi.org/10.1111/1462-2920.13642
Dickie IA, Alexander IJ, Lennon S et al (2015) Evolving insights to understanding mycorrhizas. New Phytol 205:1369–1374
Dickie IA, Reich PB (2005) Ectomycorrhizal fungal communities at forest edges. J Ecol 93:244–255. https://doi.org/10.1111/j.1365-
Fernandez CW, Nguyen NH, Stefanski A et al (2017) Ectomycorrhizal fungal response to warming is linked to poor host performance at the boreal-temperate ecotone. Glob Chang Biol 23:1598–1609. https://doi.org/10.1111/gcb.13510
Garten CT (1993) Variation in Foliar 15N abundance and the availability of soil nitrogen on Walker Branch Watershed. Ecology 74:2098–2113
Glassman SI, Wang IJ, Bruns TD (2017) Environmental filtering by pH and soil nutrients drives community assembly in fungi at fine spatial scales. Mol Ecol 26:6960–6973. https://doi.org/10.1111/mec.14414
Grigoriev IV, Nikitin R, Haridas S et al (2014) MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res 42:699–704. https://doi.org/10.1093/nar/gkt1183
Guo M, Gao G, Ding G, Zhang Y (2020) Drivers of ectomycorrhizal fungal community structure associated with Pinus sylvestris var. mongolica differ at regional vs. local spatial scales in northern China. Forests. 11:323. https://doi.org/10.3390/f11030323
Hagenbo A, Kyaschenko J, Clemmensen KE, Lindahl BD, Fransson P (2018) Fungal community shifts underpin declining mycelial production and turnover across a Pinus sylvestris chronosequence. J Ecol 106:490–501. https://doi.org/10.1111/1365-2745.12917
Hasselquist NJ, Metcalfe DB, Inselsbacher E et al (2016) Greater carbon allocation to mycorrhizal fungi reduces tree nitrogen uptake in a boreal forest. Ecology 97:1012–1022. https://doi.org/10.1890/15-1222.1
Hess J, Skrede I, Wolfe BE, LaButti K, Ohm RA, Grigoriev IV, Pringle A (2014) Transposable element dynamics among asymbiotic and ectomycorrhizal Amanita fungi. Genome Biol Evol 6:1564–1578. https://doi.org/10.1093/gbe/evu121/
Hobbie EA (2006) Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology 87:563–569. https://doi.org/10.1890/05-0755
Hobbie EA, Högberg P (2012) Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics. New Phytol 196:367–382. https://doi.org/10.1111/j.1469-8137.2012.04300.x
Ivarson KC (1977) Changes in decomposition rate, microbial population and carbohydrate content of an acid peat bog after liming and reclamation. Can J Soil Sci 57:129–137. https://doi.org/10.4141/cjss77-017
Karst J, Wasyliw J, Birch JD, Franklin J, Chang SX, Erbilgin N (2021) Long-term nitrogen addition does not sustain host tree stem radial growth but doubles the abundance of high-biomass ectomycorrhizal fungi. Glob Chang Biol 27:4125–4138. https://doi.org/10.1111/gcb.15713
Kellner H, Luis P, Pecyna MJ et al (2014) Widespread occurrence of expressed fungal secretory peroxidases in forest soils. PLoS ONE 9:e95557. https://doi.org/10.1371/journal.pone.0095557
Kennedy PG, Izzo AD, Bruns TD (2003) There is high potential for the formation of common mycorrhizal networks between understorey and canopy trees in a mixed evergreen forest. J Ecol 91:1071–1080. https://doi.org/10.1046/j.1365-2745.2003.00829.x
Kennedy PG, Mielke LA, Nguyen NH (2018) Ecological responses to forest age, habitat, and host vary by mycorrhizal type in boreal peatlands. Mycorrhiza 28:315–328. https://doi.org/10.1007/s00572-018-0821-4
Kohler A, Kuo A, Nagy LG et al (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
Koide R, Fernandez C, Petprakob K (2011) General principles in the community ecology of ectomycorrhizal fungi. Ann For Sci 68:45–55. https://doi.org/10.1007/s13595-010-0006-6
Kummel M, Lostroh P (2011) Altering light availability to the plant host determined the identity of the dominant ectomycorrhizal fungal partners and mediated mycorrhizal effects on plant growth. Botany 89:439–450. https://doi.org/10.1139/b11-033
Kyaschenko J, Clemmensen KE, Hagenbo A et al (2017) Shift in fungal communities and associated enzyme activities along an age gradient of managed Pinus sylvestris stands. ISME J 11:863–874. https://doi.org/10.1038/ismej.2016.184
Laine J, Vasander H, Laiho R (1995) Long-term effects of water level drawdown on the vegetation of drained pine mires in Southern Finland. J Appl Ecol 32:785–802. https://doi.org/10.2307/2404818
Lamit LJ, Romanowicz KJ, Potvin LR et al (2017) Patterns and drivers of fungal community depth stratification in Sphagnum peat. FEMS Microbiol Ecol 93:1–14. https://doi.org/10.1093/femsec/fix082
Leifeld J, Klein K, Wüst-Galley C (2020) Soil organic matter stoichiometry as indicator for peatland degradation. Sci Rep 10:1–9. https://doi.org/10.1038/s41598-020-64275-y
Lierop WV, Mackenzie AF (1977) Soil pH measurement and its application to organic soils. Can J Soil Sci 57:55–64. https://doi.org/10.4141/cjss77-008
Lilleskov EA, Fahey TJ, Horton TR, Lovett GM (2002) Belowground ectomycorrhizal fungal community change over a nitrogen deposition gradient in Alaska. Ecology 83:104. https://doi.org/10.2307/2680124
Lilleskov EA, Fahey TJ, Lovett GM (2001) Ectomycorrhizal fungal aboveground community change over an atmospheric nitrogen deposition gradient. Ecol Appl 11:397–410. https://doi.org/10.1890/1051-0761(2001)011[0397:EFACCO]2.0.CO;2
Lilleskov EA, Hobbie EA, Horton TR (2011) Conservation of ectomycorrhizal fungi: exploring the linkages between functional and taxonomic responses to anthropogenic N deposition. Fungal Ecol 4:174–183. https://doi.org/10.1016/j.funeco.2010.09.008
Lilleskov EA, Kuyper TW, Bidartondo MI, Hobbie EA (2019) Atmospheric nitrogen deposition impacts on the structure and function of forest mycorrhizal communities: a review. Environ Pollut. https://doi.org/10.1016/j.envpol.2018.11.074
Lindahl BD, Tunlid A (2015) Ectomycorrhizal fungi – potential organic matter decomposers, yet not saprotrophs. New Phytol 205:1443–1447
Lofgren LA, Nguyen NH, Vilgalys R et al (2021) Comparative genomics reveals dynamic genome evolution in host specialist ectomycorrhizal fungi. New Phytol 230:774–792. https://doi.org/10.1111/nph.17160
Luo T, Pan Y, Ouyang H et al (2004) Leaf area index and net primary productivity along subtropical to alpine gradients in the Tibetan Plateau. Glob Ecol Biogeogr 13:345–358. https://doi.org/10.1111/j.1466-822X.2004.00094.x
Martin F, Aerts A, Ahrén D et al (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:88–92. https://doi.org/10.1038/nature06556
Martin F, Kohler A, Murat C et al (2016) Unearthing the roots of ectomycorrhizal symbioses. Nat Rev Microbiol 14:760–773. https://doi.org/10.1038/nrmicro.2016.149
Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet J 17(10–17):20
Martino E, Morin E, Grelet GA et al (2018) Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists. New Phytol 217:1213–1229. https://doi.org/10.1111/nph.14974
Miyauchi S (2020) Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits. Nat Commun 11:5125. https://doi.org/10.1038/s41467-020-18795-w
Nguyen NH, Song Z, Bates ST et al (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
Nilsson RH, Larsson KH, Taylor AFS et al (2019) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res 47:D259–D264. https://doi.org/10.1093/nar/gky1022
Oksanen J, Blanchet FG, Friendly M et al (2018) vegan: Community Ecology Package. R package version 2.5-7. https://CRAN.R-project.org/package=vegan. Accessed 3 Mar 2020
Page SE, Rieley JO, Banks CJ (2011) Global and regional importance of the tropical peatland carbon pool. Glob Chang Biol 17:798–818. https://doi.org/10.1111/j.1365-2486.2010.02279.x
Parker TC, Sadowsky J, Dunleavy H et al (2017) Slowed biogeochemical cycling in sub-arctic birch forest linked to reduced mycorrhizal growth and community change after a defoliation event. Ecosystems 20:316–330. https://doi.org/10.1007/s10021-016-0026-7
Peay KG, Garbelotto M, Bruns TD (2010) Evidence of dispersal limitation in soil microorganisms: isolation reduces species richness on mycorrhizal tree islands. Ecology 91:3631–3640. https://doi.org/10.1890/09-2237.1
Peter M, Kohler A, Ohm RA et al (2016) Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum. Nat Commun 7:12662. https://doi.org/10.1038/ncomms12662
Philben M, Kaiser K, Benner R (2014) Does oxygen exposure time control the extent of organic matter decomposition in peatlands? J Geophys Res Biogeosciences 119:897–909. https://doi.org/10.1002/2013JG002573
Potila H, Wallander H, Sarjala T (2009) Growth of ectomycorrhizal fungi in drained peatland forests with variable P and K availability. Plant Soil 316:139–150. https://doi.org/10.1007/s11104-008-9766-2
Potvin LR, Kane ES, Chimner RA et al (2015) Effects of water table position and plant functional group on plant community, aboveground production, and peat properties in a peatland mesocosm experiment (PEATcosm). Plant Soil 387:277–294. https://doi.org/10.1007/s11104-014-2301-8
Poznanovic SK, Lilleskov EA, Webster CR (2014) Sharing rotting wood in the shade: ectomycorrhizal communities of co-occurring birch and hemlock seedlings. Mycorrhiza 25:153–164. https://doi.org/10.1007/s00572-014-0597-0
Richard F, Millot S, Gardes M, Selosse MA (2005) Diversity and specificity of ectomycorrhizal fungi retrieved from an old-growth Mediterranean forest dominated by Quercus ilex. New Phytol 166:1011–1023. https://doi.org/10.1111/j.1469-8137.2005.01382.x
Rivers AR, Weber KC, Gardner TG et al (2018) ITSxpress: software to rapidly trim internally transcribed spacer sequences with quality scores for marker gene analysis [version 1; peer review: 2 approved]. F1000Research 7. https://doi.org/10.12688/F1000RESEARCH.15704.1
Rosinger C, Sandén H, Matthews B et al (2018) Patterns in ectomycorrhizal diversity, community composition, and exploration types in European beech, pine, and spruce forests. Forests 9:f9080445. https://doi.org/10.3390/f9080445
Rosseel Y (2012) lavaan: an R Package for Structural Equation Modeling. J Stat Softw 48:1–36
Ryberg M, Matheny PB (2012) Asynchronous origins of ectomycorrhizal clades of Agaricales. Proc R Soc B 279:3465–3473. https://doi.org/10.1098/rspb.201
Selosse M-A, Richard F, He X, Simard SW (2006) Mycorrhizal networks: des liaisons dangereuses? Trends Ecol Evol. 21:621–628. https://doi.org/10.1016/j.tree.2006.07.003
Smith SE, Read D (2008) Mycorrhizal symbiosis (Third Edition), 3rd edn. Academic Press, New York, NY
Stanek W (1961) Natural layering of black spruce in northern Ontario. Forest Chron 37:245–258. https://doi.org/10.5558/tfc37245-3
Sterkenburg E, Bahr A, Brandstr M, Clemmensen KE (2015) Changes in fungal communities along a boreal forest soil fertility gradient. New Phytol 207:1–14. https://doi.org/10.1111/nph.13426
Stuart EK, Plett KL (2020) Digging deeper. In Search of the mechanisms of carbon and nitrogen exchange in ectomycorrhizal symbioses. Front Plant Sci 10:1–11. https://doi.org/10.3389/fpls.2019.01658
Talbot JM, Bruns TD, Taylor JW et al (2014) Endemism and functional convergence across the North American soil mycobiome. Proc Natl Acad Sci 111:6341–6346. https://doi.org/10.1073/pnas.1402584111
Taylor DL, Walters WA, Lennon NJ et al (2016) Accurate estimation of fungal diversity and abundance through improved lineage-specific primers optimized for Illumina amplicon sequencing. Appl Environ Microbiol 82:3–4. https://doi.org/10.1128/AEM.02576-16
Team RC (2018)Â R: a language and environment for statistical computing. Version 3.5.0. R Foundation for Statistical Computing, Vienna, Austra. Available from http://www.R-project.org. Accessed 10 Feb 2020
Tedersoo L, Anslan S, Bahram M et al (2020) Regional-scale in-depth analysis of soil fungal diversity reveals strong pH and plant species effects in northern Europe. Front Microbiol 11:1–31. https://doi.org/10.3389/fmicb.2020.01953
Thoen E, Harder CB, Kauserud H et al (2020) In vitro evidence of root colonization suggests ecological versatility in the genus Mycena. New Phytol 227:601–612. https://doi.org/10.1111/nph.16545
Thomson AM, Brown RA, Rosenberg NJ et al (2005) Climate change impacts for the conterminous USA: an integrated assessment. Part 4. Water Resources Clim Chang 69:67–88. https://doi.org/10.1007/1-4020-3876-3
Toberman H, Laiho R, Evans CD et al (2010) Long-term drainage for forestry inhibits extracellular phenol oxidase activity in Finnish boreal mire peat. Eur J Soil Sci 61:950–957. https://doi.org/10.1111/j.1365-2389.2010.01292.x
von Post L (1924) Das genetische System der organogenen Bildungen Schwedens. International Committee of Soil Science 1924:287–304
Watt RF, Heinselman ML (1965) Foliar nitrogen and phosphorus level related to site quality in a Northern Minnesota Spruce Bog. Ecology 46:357–361
Weber R, Schwendener A, Schmid S et al (2018) Living on next to nothing: tree seedlings can survive weeks with very low carbohydrate concentrations. New Phytol. https://doi.org/10.1111/nph.14987
Westman CJ, Laiho R (2003) Nutrient dynamics of drained peatland forests. Biogeochemistry 63:269–298. https://doi.org/10.1023/A:1023348806857
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
Wiedermann MM, Kane ES, Potvin LR, Lilleskov EA (2017) Interactive plant functional group and water table effects on decomposition and extracellular enzyme activity in Sphagnum peatlands. Soil Biol Biochem 108:1–8. https://doi.org/10.1016/j.soilbio.2017.01.008
Wilson RM, Tfaily MM, Kolton M et al (2021) Soil metabolome response to whole-ecosystem warming at the Spruce and Peatland Responses under Changing Environments experiment. Proc Natl Acad Sci 118:e20044192118. https://doi.org/10.1073/pnas.2004192118
Yu ZC (2012) Northern peatland carbon stocks and dynamics: a review. Biogeosciences 9:4071–4085. https://doi.org/10.5194/bg-9-4071-2012
Zheng W, Lehmann A, Ryo M et al (2020) Growth rate trades off with enzymatic investment in soil filamentous fungi. Sci Rep 10. https://doi.org/10.1101/360511
Acknowledgements
We thank Lela Andrews from the Northern Arizona University Environmental Genetics and Genomics Laboratory (EnGGen) for assistance with Illumina sequencing and bioinformatics. We also thank Jamie Lamit for bioinformatics assistance. Claire Hendricks, Kaitlyn Dodge, Dominic Uhelski, Jesse Barta, Rachel Sperry, Monica Heirman, Kevin McConnell, Evan Kane, Jennifer Eikenberry, Kristin Brzeski, and Chris Webster provided field and laboratory assistance. This research was conducted on ancestral Anishinaabe homelands.
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SFH was supported by grants from the USDA-NIFA McIntire Stennis Cooperative Forestry Research Program (to Yvette L. Dickinson) and a Doctoral Finishing Fellowship from Michigan Technological University.
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Hupperts, S.F., Lilleskov, E.A. Predictors of taxonomic and functional composition of black spruce seedling ectomycorrhizal fungal communities along peatland drainage gradients. Mycorrhiza 32, 67–81 (2022). https://doi.org/10.1007/s00572-021-01060-3
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DOI: https://doi.org/10.1007/s00572-021-01060-3
Keywords
- Ectomycorrhiza
- Peatlands
- Boreal
- Picea mariana
- Cortinarius