Abstract
Aims
While fungi are key drivers of the carbon cycle and obligate symbionts of trees, the link between plant-fungal interactions and landscape vegetation changes has been largely overlooked. Our aim was to test whether a local difference in dominant tree species would shape the composition of soil fungi communities.
Methods
Fungal communities were described using next-generation DNA sequencing. Composite soil samples were collected in four paired sites (represented by one pure aspen stand and one pure spruce stand) and soil nutriments were measured.
Results
Of the more than 1119 OTUs, 31.6% were Ascomycota while 27.8% were Basidiomycota, 15% were ectomycorrhizal fungi whereas 19.7% were saprotrophic. Communities displayed high species turnover among forest types rather than differences in species richness. Among tested predictors, the dominant tree species explained around 11% of fungal community variation. pH and soil nutrients were also strong predictors of fungal communities.
Conclusions
Our study revealed strong correlations between dominant tree species and fungal communities at a local scale and raised questions regarding the impact of fungal communities on forest soil nutrient dynamics.
This is a preview of subscription content, access via your institution.



References
Abarenkov K, Tedersoo L, Nilsson RH, Vellak K, Saar I, Veldre V, Parmasto E, Prous M, Aan A, Ots M, Kurina O, Ostonen I, Jõgeva J, Halapuu S, Põldmaa K, Toots M, Truu J, Larsson K-H, Kõljalg U (2010) PlutoF—a web based workbench for ecological and taxonomic research, with an online implementation for fungal ITS sequences, PlutoF—a Web Based Workbench for Ecological and Taxonomic Research, with an Online Implementation for Fungal ITS Sequences. Evol Bioinforma 6:189–196. https://doi.org/10.4137/EBO.S6271
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Arbour M-L, Bergeron Y (2011) Effect of increased Populus cover on Abies regeneration in the Picea-feathermoss boreal forest. J Veg Sci 22:1132–1142. https://doi.org/10.1111/j.1654-1103.2011.01314.x
Bahram M, Harend H, Tedersoo L (2014) Network perspectives of ectomycorrhizal associations. Fungal Ecol 7:70–77. https://doi.org/10.1016/j.funeco.2013.10.003
Bardgett RD, Wardle DA (2010) Aboveground-belowground linkages: biotic interactions, ecosystem processes, and global change. Oxford University Press, Oxford
Bennett JA, Maherali H, Reinhart KO, Lekberg Y, Hart MM, Klironomos J (2017) Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355:181–184. https://doi.org/10.1126/science.aai8212
Bent E, Kiekel P, Brenton R, Taylor DL (2011) Root-associated ectomycorrhizal Fungi shared by various boreal Forest seedlings naturally regenerating after a fire in interior Alaska and correlation of different Fungi with host growth responses. Appl Environ Microbiol 77:3351–3359. https://doi.org/10.1128/AEM.02575-10
Booth MG (2004) Mycorrhizal networks mediate overstorey-understorey competition in a temperate forest: mycorrhizal networks and plant competition. Ecol Lett 7:538–546. https://doi.org/10.1111/j.1461-0248.2004.00605.x
Boyer F, Mercier C, Bonin A, Le Bras Y, Taberlet P, Coissac E (2016) obitools : a unix-inspired software package for DNA metabarcoding. Mol Ecol Resour 16:176–182. https://doi.org/10.1111/1755-0998.12428
Brandt JP, Flannigan MD, Maynard DG, Thompson ID, Volney WJA (2013) An introduction to Canada’s boreal zone: ecosystem processes, health, sustainability, and environmental issues. Environ Rev 21:207–226. https://doi.org/10.1139/er-2013-0040
Carter MR, Gregorich EG (eds) (2008) Soil sampling and methods of analysis, second edn. Canadian Society of Soil Science. CRC Press, Boca Raton, FL, USA
Cavard X, Bergeron Y, Chen HYH, Paré D (2011) Effect of forest canopy composition on soil nutrients and dynamics of the understorey: mixed canopies serve neither vascular nor bryophyte strata. J Veg Sci 22:1105–1119. https://doi.org/10.1111/j.1654-1103.2011.01311.x
Chao A, Lee S-M (1992) Estimating the number of classes via sample coverage. J Am Stat Assoc 87:210–217. https://doi.org/10.1080/01621459.1992.10475194
Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD (2013) Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339:1615–1618. https://doi.org/10.1126/science.1231923
Davey ML, Currah RS (2006) Interactions between mosses (Bryophyta) and fungi. Can J Bot 84:1509–1519. https://doi.org/10.1139/b06-120
Davey ML, Skogen MJ, Heegaard E, Halvorsen R, Kauserud H, Ohlson M (2017) Host and tissue variations overshadow the response of boreal moss-associated fungal communities to increased nitrogen load. Mol Ecol 26:571–588. https://doi.org/10.1111/mec.13938
Drobyshev I, Gewehr S, Berninger F, Bergeron Y (2013) Species-specific growth responses of black spruce and trembling aspen may enhance resilience of boreal forest to climate change. J Ecol 101:231–242. https://doi.org/10.1111/1365-2745.12007
Environment Canada (2017) Canadian climate normals 1971-2000. Environment Canada, National Meteorological Service, Downsview, ON. Accessed November 2017. http://climate.weatheroffice.gc.ca/climate_normals/index_e.html
Epp LS, Boessenkool S, Bellemain EP, Haile J, Esposito A, Riaz T, Erséus C, Gusarov VI, Edwards ME, Johnsen A, Stenøien HK, Hassel K, Kauserud H, Yoccoz NG, Bråthen KA, Willerslev E, Taberlet P, Coissac E, Brochmann C (2012) New environmental metabarcodes for analysing soil DNA: potential for studying past and present ecosystems. Mol Ecol 21:1821–1833. https://doi.org/10.1111/j.1365-294X.2012.05537.x
Fenton NJ, Bergeron Y (2006) Facilitative succession in a boreal bryophyte community driven by changes in available moisture and light. J Veg Sci 17:65–76. https://doi.org/10.1111/j.1654-1103.2006.tb02424.x
Fenton NJ, Bergeron Y (2008) Does time or habitat make old-growth forests species rich? Bryophyte richness in boreal Picea mariana forests. Biol Conserv 141:1389–1399. https://doi.org/10.1016/j.biocon.2008.03.019
Fernandez CW, Nguyen N, Stefański A, Han Y, Hobbie SE, Montgomery RA, Reich PB, Kennedy PG (2017) Ectomycorrhizal fungal response to warming is linked to poor host performance at the boreal-temperate ecotone. Glob Change Biol 23(4):1598–1609. https://doi.org/10.1111/gcb.13510
Foudyl-Bey S, Brais S, Drouin P (2016) Litter heterogeneity modulates fungal activity, C mineralization and N retention in the boreal forest floor. Soil Biol Biochem 100:264–275. https://doi.org/10.1016/j.soilbio.2016.06.017
Gagnon R (1989) Maintien après feu de limites abruptes entre des peuplements d’épinettes noires (Picea mariana) et des formations de feuillus intolérants (Populus tremuloides et Betula papyrifera) dans la région du Saguenay–Lac-Saint-Jean (Québec). Nat Can 116:117–124
Gauthier S, Bernier P, Kuuluvainen T, Shvidenko AZ, Schepaschenko DG (2015) Boreal forest health and global change. Science 349:819–822. https://doi.org/10.1126/science.aaa9092
Hirose D, Hobara S, Matsuoka S, Kato K, Tanabe Y, Uchida M, Kudoh S, Osono T (2016) Diversity and community assembly of moss-associated fungi in ice-free coastal outcrops of continental Antarctica. Fungal Ecol 24:94–101. https://doi.org/10.1016/j.funeco.2016.09.005
Ishida TA, Nara K, Hogetsu T (2007) Host effects on ectomycorrhizal fungal communities: insight from eight host species in mixed conifer–broadleaf forests. New Phytol 174:430–440. https://doi.org/10.1111/j.1469-8137.2007.02016.x
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
Kyaschenko J, Clemmensen KE, Karltun E, Lindahl BD (2017) Below-ground organic matter accumulation along a boreal forest fertility gradient relates to guild interaction within fungal communities. Ecol Lett 20:1546–1555. https://doi.org/10.1111/ele.12862
Laquerre S, Harvey BD, Leduc A (2011) Spatial analysis of response of trembling aspen patches to clearcutting in black spruce-dominated stands. For Chron 87:77–85. https://doi.org/10.5558/tfc87077-1
Légaré S, Paré D, Bergeron Y (2005) Influence of aspen on forest floor properties in black spruce-dominated stands. Plant Soil 275:207–220. https://doi.org/10.1007/s11104-005-1482-6
Lindahl BO, Taylor AFS, Finlay RD (2002) Defining nutritional constraints on carbon cycling in boreal forests – towards a less `phytocentric’ perspective. Plant Soil 242:123–135. https://doi.org/10.1023/A:1019650226585
Mehlich A (1984) Mehlich 3 soil test extractant: a modification of Mehlich 2 extractant. Commun Soil Sci Plant Anal 15:1409–1416. https://doi.org/10.1080/00103628409367568
Messaoud Y, Bergeron Y, Asselin H (2007a) Reproductive potential of balsam fir (Abies balsamea), white spruce (Picea glauca), and black spruce (P. mariana) at the ecotone between mixedwood and coniferous forests in the boreal zone of western Quebec. Am J Bot 94:746–754. https://doi.org/10.3732/ajb.94.5.746
Messaoud Y, Bergeron Y, Leduc A (2007b) Ecological factors explaining the location of the boundary between the mixedwood and coniferous bioclimatic zones in the boreal biome of eastern North America. Glob Ecol Biogeogr 16:90–102. https://doi.org/10.1111/j.1466-8238.2006.00277.x
Molina R, Massicotte H, Trappe JM (1992) Specificity phenomena in mycorrhizal symbioses: community-ecological consequences and practical implications. In: Allen MF (ed.). Mycorrhizal functioning: an integrative plant-fungal process.Chapman & Hall, London. pp. 357–423
Mucha J, Peay KG, Smith DP, Reich PB, Stefański A, Hobbie SE (2018) Effect of simulated climate warming on the ectomycorrhizal fungal Community of Boreal and Temperate Host Species Growing near Their Shared Ecotonal Range Limits. Microb Ecol 75:348–363. https://doi.org/10.1007/s00248-017-1044-5
Nara K, Hogetsu T (2004) Ectomycorrhizal fungi on established shrubs facilitate subsequent seedling establishment of successional plant species. Ecology 85:1700–1707. https://doi.org/10.1890/03-0373
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
Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N, Larsson K-H (2008) Intraspecific ITS variability in the kingdom Fungi as expressed in the international sequence databases and ITS implications for molecular species identification. Evol Bioinformatics Online 4:193–201
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) Vegan: community ecology package. R package version 2:4–5. https://cran.r-project. .org/package=vegan
Pan Y, Birdsey RA, Fang J, Houghton R, Kauppi PE, Kurz WA, Phillips OL, Shvidenko A, Lewis SL, Canadell JG, Ciais P, Jackson RB, Pacala SW, McGuire AD, Piao S, Rautiainen A, Sitch S, Hayes D (2011) A large and persistent carbon sink in the world’s forests. Science 333:988–993. https://doi.org/10.1126/science.1201609
R Core Team. 2015. R: A language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria. https://www.R-project.org/
Read DJ, Leake JR, Perez-Moreno J (2004) Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Can J Bot 82:1243–1263. https://doi.org/10.1139/b04-123
Robitaille A, Saucier J-P (1996) Land district, ecophysiographic units and areas: the landscape mapping of the ministère des ressources naturelles du Québec. In: global to local: ecological land classification. Springer, Dordrecht, pp 127–148
Santalahti M, Sun H, Jumpponen A, Pennanen T, Heinonsalo J (2016) Vertical and seasonal dynamics of fungal communities in boreal scots pine forest soil. FEMS Microbiol Ecol 92:fiw170. https://doi.org/10.1093/femsec/fiw170
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
Shi L-L, Mortimer PE, Slik JWF, Zou X-M, Xu J, Feng W-T, Qiao L (2014) Variation in forest soil fungal diversity along a latitudinal gradient. Fungal Divers 64:305–315. https://doi.org/10.1007/s13225-013-0270-5
Simard M, Lecomte N, Bergeron Y, Bernier PY, Paré D (2007) Forest productivity decline caused by successional paludification of boreal soils. Ecol Appl 17:1619–1637. https://doi.org/10.1890/06-1795.1
Smith JE, Molina R, Huso MM, Luoma DL, McKay D, Castellano MA, Lebel T, Valachovic Y (2002) Species richness, abundance, and composition of hypogeous and epigeous ectomycorrhizal fungal sporocarps in young, rotation-age, and old-growth stands of Douglas-fir (Pseudotsuga menziesii) in the Cascade Range of Oregon, U.S.A. Can J Bot 80:186–204. https://doi.org/10.1139/b02-003
Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A, James TY, O’Donnell K, Roberson RW, Taylor TN, Uehling J, Vilgalys R, White MM, Stajich JE (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046. https://doi.org/10.3852/16-042
Taudiere A, Munoz F, Lesne A, Monnet A-C, Bellanger J-M, Selosse M-A, Moreau P-A, Richard F (2015) Beyond ectomycorrhizal bipartite networks: projected networks demonstrate contrasted patterns between early- and late-successional plants in Corsica. Front Plant Sci 6:881. https://doi.org/10.3389/fpls.2015.00881
Taylor DL, Herriott IC, Stone KE, McFarland JW, Booth MG, Leigh MB (2010) Structure and resilience of fungal communities in Alaskan boreal forest soils. Can J For Res 40:1288–1301. https://doi.org/10.1139/X10-081
Taylor DL, Hollingsworth TN, McFarland JW, Lennon NJ, Nusbaum C, Ruess RW (2013) 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, Dickie IA (2014) Does host plant richness explain diversity of ectomycorrhizal fungi? Re-evaluation of Gao et al. (2013) data sets reveals sampling effects. Mol Ecol 23:992–995. https://doi.org/10.1111/mec.12660
Tedersoo L, Bahram M, Toots M, Diédhiou 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 21:4160–4170. https://doi.org/10.1111/j.1365-294X.2012.05602.x
Thormann MN (2006) The role of fungi in boreal peatlands. In: Wieder RK, Vitt DH (eds) Boreal peatland ecosystems. Springer, Berlin Heidelberg, pp 101–123
Treseder KK, Bent E, Borneman J, McGuire KL (2014) Shifts in fungal communities during decomposition of boreal forest litter. Fungal Ecol 10:58–69. https://doi.org/10.1016/j.funeco.2013.02.002
Truong C, Mujic AB, Healy R, Kuhar F, Furci G, Torres D, Niskanen T, Sandoval-Leiva PA, Fernández N, Escobar JM, Moretto A, Palfner G, Pfister D, Nouhra E, Swenie R, Sánchez-García M, Matheny PB, Smith ME (2017) How to know the fungi: combining field inventories and DNA-barcoding to document fungal diversity. New Phytol 214:913–919. https://doi.org/10.1111/nph.14509
Twieg BD, Durall DM, Simard SW (2007) Ectomycorrhizal fungal succession in mixed temperate forests. New Phytol 176:437–447. https://doi.org/10.1111/j.1469-8137.2007.02173.x
White, T.J., Bruns TD, Lee SB, Taylor J, AM Innis , H Gelfand D, Sninsky J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, DH Gelfand DH, Sninsky JJ, White TJ (eds). PCR protocols: a guide to methods and applications. Academic Press, New York. pp. 315–322
Acknowledgements
The authors sincerely thank Evick Mestre, Danielle Charon and Raynald Julien for their assistance in the field, Francine Tremblay for laboratory access, Lucie Zinger for assistance with bioinformatics and sequence analyses, Benjamin Durrington for editing the text and WFJ Parsons for English revision. We are grateful to our internal reviewer, Julien Demenois (CIRAD), for helpful advice and comments on a previous version of the manuscript. We are grateful to the Genotoul Bioinformatics Platform, Toulouse Midi-Pyrenees, for providing computing and storage resources. We also thank two anonymous reviewers and section editor Thomas W. Kuyper for their relevant and helpful comments on previous versions of the manuscript.
Funding
This work was supported by Mitacs Acceleration in collaboration with Norbord Inc. [IT066831], the UQAT-UQAM-NSERC Chair in sustainable forest management, the French Laboratory of Excellence project “TULIP” (ANR-10-LABX-41; ANR-11-IDEX-0002-02), and University Paul Sabatier for travel fellowships.
Author information
Affiliations
Corresponding author
Additional information
Responsible Editor: Thom W. Kuyper
Electronic supplementary material
ESM 1
(DOCX 10 kb)
Rights and permissions
About this article
Cite this article
Nagati, M., Roy, M., Manzi, S. et al. Impact of local forest composition on soil fungal communities in a mixed boreal forest. Plant Soil 432, 345–357 (2018). https://doi.org/10.1007/s11104-018-3806-3
Received:
Accepted:
Published:
Issue Date:
Keywords
- Black spruce-feather moss
- Fungal diversity
- Soil ecology
- Picea mariana
- Populus tremuloides
- NGS