Microbial Ecology

, Volume 73, Issue 3, pp 521–531 | Cite as

Experimental Climate Change Modifies Degradative Succession in Boreal Peatland Fungal Communities

  • Asma Asemaninejad
  • R. Greg Thorn
  • Zoë LindoEmail author
Fungal Microbiology


Peatlands play an important role in global climate change through sequestration of atmospheric CO2. Climate-driven changes in the structure of fungal communities in boreal peatlands that favor saprotrophic fungi can substantially impact carbon dynamics and nutrient cycling in these crucial ecosystems. In a mesocosm study using a full factorial design, 100 intact peat monoliths, complete with living Sphagnum and above-ground vascular vegetation, were subjected to three climate change variables (increased temperature, reduced water table, and elevated CO2 concentrations). Peat litterbags were placed in mesocosms, and fungal communities in litterbags were monitored over 12 months to assess the impacts of climate change variables on peat-inhabiting fungi. Changes in fungal richness, diversity, and community composition were assessed using Illumina MiSeq sequencing of ribosomal DNA (rDNA). While general fungal richness reduced under warming conditions, Ascomycota exhibited higher diversity under increased temperature treatments over the course of the experiment. Both increased temperature and lowered water table position drove shifts in fungal community composition with a strong positive effect on endophytic and mycorrhizal fungi (including one operational taxonomic unit (OTU) tentatively identified as Barrenia panicia) and different groups of saprotrophs identified as Mortierella, Galerina, and Mycena. These shifts were observed during a predicted degradative succession in the decomposer community as different carbon substrates became available. Since fungi play a central role in peatland communities, increased abundances of saprotrophic fungi under warming conditions, at the expense of reduced fungal richness overall, may increase decomposition rates under future climate scenarios and could potentially aggravate the impacts of climate change.


Ascomycota Climate change Degradative succession Fungi Illumina MiSeq Peatlands 



Basic Local Alignment Search Tool


Large subunit


Next generation sequencing


Operational taxonomic unit


Polymerase chain reaction


Ribosomal DNA


Principal component analysis


Analysis of variance


ANOVA-like differential expression procedure


Microbiome Regression-based Kernel Association Test



The authors thank two anonymous reviewers for their thoughtful and constructive comments on previous versions of this manuscript. We also thank Dr. Charmaine Dean, Dean of the Faculty of Science, University of Western Ontario, for her financial assistance to use Biotron and the financial support provided by the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant program awarded to Dr. Zoë Lindo and Dr. Brian Branfireun. We are grateful to Dr. Greg Gloor (Western University, Biochemistry) for bioinformatics and statistical assistance to and David Carter (Roberts Research Institute) for conducting Illumina sequencing. We thank the volunteers and work study students for their help in the lab. Discussion with Dr. Hugh Henry, Dr. Marc-Andre Lachance, Nimalka Weerasuriya, and Dr. Catherine Dieleman are appreciated.

Supplementary material

248_2016_875_MOESM1_ESM.pdf (131 kb)
Supplementary Fig. 1 Changes in the relative frequencies of Ascomycota a and other fungal community b at higher taxonomic levels (classes) observed at different time points of the experiment. (PDF 130 kb)
248_2016_875_MOESM2_ESM.pdf (138 kb)
(PDF 138 kb)
248_2016_875_MOESM3_ESM.docx (21 kb)
ESM 1 (DOCX 21 kb)


  1. 1.
    Clymo RS, Turunen J, Tolonen K (1998) Carbon accumulation in peatland. Oikos 81:368–388CrossRefGoogle Scholar
  2. 2.
    Gorham E (1991) Northern peatlands: role in the carbon cycle and probable responses to climatic warming. Ecol Appl 1:182–195CrossRefPubMedGoogle Scholar
  3. 3.
    Moore T, Basiliko N (2006) Decomposition in boreal peatlands. In: Wieder RK, Vitt DH (eds) Boreal peatland ecosystems. Ecological studies, vol 188. Springer, Berlin, pp 125–143CrossRefGoogle Scholar
  4. 4.
    IPCC (2014) Climate change 2013: the physical science basis: Working Group I Contribution to the Fifth Assessment Report of the International Panel on Climate Change. Cambridge University Press, LondonGoogle Scholar
  5. 5.
    Frolking S, Roulet NT (2007) Holocene radiative forcing impact of northern peatland carbon accumulation and methane emissions. Glob Chang Biol 13:1079–1088CrossRefGoogle Scholar
  6. 6.
    Williams RT, Crawford RL (1983) Microbial diversity of Minnesota peatlands. Microb Ecol 9:201–214CrossRefPubMedGoogle Scholar
  7. 7.
    Andersen R, Chapman SS, Artez RRE (2013) Microbial communities in natural and disturbed peatlands: a review. Soil Biol Biochem 57:979–994CrossRefGoogle Scholar
  8. 8.
    Treseder KK, Marusenko Y, Romero-Olivares AL, Maltz MR (2016) Experimental warming alters potential function of the fungal community in boreal forest. Glob Chang Biol. doi: 10.1111/gcb.13238 PubMedGoogle Scholar
  9. 9.
    Allison SD, Treseder KK (2011) Climate change feedbacks to microbial decomposition in boreal soils. Fungal Ecol 4:362–374CrossRefGoogle Scholar
  10. 10.
    Kasurinen A, Peltonen PA, Holopainen JK, Vapaauori E, Holocaine T (2007) Leaf litter under changing climate: will increasing levels of CO2 and O3 affect decomposition and nutrient cycling processes? Dyn Soil Dyn Plant 1:58–67Google Scholar
  11. 11.
    Trinder CJ, Artz RRE, Johnson D (2008) Interactions between fungal community structure, litter decomposition and depth of water-table in a cutover peatland. FEMS Microbiol Ecol 64:433–448CrossRefPubMedGoogle Scholar
  12. 12.
    Yuste JC, Penuelas J, Estiarte M et al (2011) Drought‐resistant fungi control soil organic matter decomposition and its response to temperature. Glob Chang Biol 17:1475–1486CrossRefGoogle Scholar
  13. 13.
    Bradford MA, Davies CA, Frey SD et al (2008) Thermal adaptation of soil microbial respiration to elevated temperature. Ecol Lett 11:1316–1327CrossRefPubMedGoogle Scholar
  14. 14.
    Drigo B, Kowalchuk GA, Van Veen JA (2008) Climate change goes underground: effects of elevated atmospheric CO2 on microbial community structure and activities in the rhizosphere. Biol Fertil Soils 44:667–679CrossRefGoogle Scholar
  15. 15.
    Peltoniemi K, Fritze H, Laiho R (2009) Response of fungal and actinobacterial communities to water-level drawdown in boreal peatland sites. Soil Biol Biochem 41:1902–1914CrossRefGoogle Scholar
  16. 16.
    Thormann MN, Currah RS, Bayley S (1999) The mycorrhizal status of the dominant vegetation along a peatland gradient in southern boreal Alberta, Canada. Wetlands 19:438–450CrossRefGoogle Scholar
  17. 17.
    Thormann MN, Currah RS, Bayley SE (2004) Patterns of distribution of microfungi in decomposing bog and fen plants. Can J Bot 82:710–710CrossRefGoogle Scholar
  18. 18.
    Thorn RG, Reddy CA, Harris D, Paul EA (1996) Isolation of saprophytic basidiomycetes from soil. Appl Environ Microbiol 62:4288–4292PubMedPubMedCentralGoogle Scholar
  19. 19.
    Tedersoo L, Lindahl BD (2016) Fungal identification biases in microbiome project. Environ Microbiol Rep. doi: 10.1111/1758-2229.12438 PubMedGoogle Scholar
  20. 20.
    Elliott DR, Caporn SJM, Nwaishi F, Nilsson RH, Sen R (2015) Bacterial and fungal communities in a degraded ombrotrophic peatland undergoing natural and managed re-vegetation. PLoS One 10(5):e0124726CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Dieleman CM, Branfireun BA, McLaughlin JW, Lindo Z (2015) Climate change drives a shift in peatland ecosystem plant community: implications for ecosystem function and stability. Glob Chang Biol 21:388–395CrossRefPubMedGoogle Scholar
  22. 22.
    Dieleman CM, Lindo Z, McLaughlin JW, Craig AE, Branfireun BA (2016) Climate change effects on peatland decomposition and porewater dissolved organic carbon biogeochemistry. Biogeochemistry. doi: 10.1007/s10533-016-0214-8 Google Scholar
  23. 23.
    Lindo Z (2015) Warming favours small-bodied organisms through enhanced reproduction and compositional shifts in belowground systems. Soil Biol Biochem 91:271–278CrossRefGoogle Scholar
  24. 24.
    Asemaninejad A, Weerasuriya N, Gloor GB, Lindo Z, Thorn RG (2016) New primers for discovering fungal diversity using nuclear large ribosomal DNA. PLoS One 11(7):e0159043CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Webster KL, McLaughlin JW (2010) Importance of the water table in controlling dissolved carbon along a fen nutrient gradient. Soil Sci Soc Am J 74:2254–2266CrossRefGoogle Scholar
  26. 26.
    Faubert P, Rochefort L (2002) Response of peatland mosses to burial by wind-dispersed peat. Bryologist 105:96–103CrossRefGoogle Scholar
  27. 27.
    Masella AP, Bartram AK, Truszkowski JM, Brown DG, Neufeld JD (2012) PANDAseq: paired-end assembler for Illumina sequences. BMC Bioinf 13:31CrossRefGoogle Scholar
  28. 28.
    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461CrossRefPubMedGoogle Scholar
  30. 30.
    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Lan Y, Wang Q, Cole JR, Rosen GL (2012) Using the RDP classifier to predict taxonomic novelty and reduce the search space for finding novel organisms. PLoS One 7:e32491CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Heck KL Jr, van Belle G, Simberloff D (1975) Explicit calculation of the rarefaction diversity measurement and the determination of sufficient sample size. Ecology 56(6):1459–146CrossRefGoogle Scholar
  33. 33.
    Statistica (version 7.0) StatSoft Inc (2004) Statistica (Data Analysis Software System), Version 7.0. Tulsa, USAGoogle Scholar
  34. 34.
    Aitchison J, Egozcue JJ (2005) Compositional data analysis: where are we and where should we be heading? Math Geol 37:829–850CrossRefGoogle Scholar
  35. 35.
    Lovell D, Pawlowsky-Glahn V, Egozcue JJ, Marguerat S, Bahler J (2015) Proportionality: a valid alternative to correlation for relative data. PLoS Comput Biol 11(3):e1004075CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    van den Boogaart KG, Tolosana-Delgado R (2008) “Compositions”: a unified r package to analyze compositional data. Comput Geosci 34:320–338CrossRefGoogle Scholar
  37. 37.
    Zhao N, Chen J, Carroll IM et al (2015) Testing in microbiome-profiling studies with MiRKAT, the Microbiome Regression-Based Kernel Association Test. Am J Hum Genet 96:797–807CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Fernandes AD, Macklaim JM, Linn TG, Reid G, Gloor GB (2013) ANOVA-like differential expression (ALDEx) analysis for mixed population RNA-Seq. PLoS One 8(7):e67019CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300Google Scholar
  40. 40.
    Belyea LR (1996) Separating the effects of litter quality and microenvironment on decomposition rates in a patterned peatland. Oikos 77:529–539CrossRefGoogle Scholar
  41. 41.
    Janssens IA, Davidson EA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173CrossRefPubMedGoogle Scholar
  42. 42.
    Wang H, Richardson CJ, Ho M (2015) Dual controls on carbon loss during drought in peatlands. Nat Clim Chang 5:584–587CrossRefGoogle Scholar
  43. 43.
    Osono T (2005) Colonization and succession of fungi during decomposition of Swida controversa leaf litter. Mycologia 97:589–597CrossRefPubMedGoogle Scholar
  44. 44.
    Adair EC, Parton WJ, Del Grosso SJ et al (2008) Simple three-pool model accurately describes patterns of long-term litter decomposition in diverse climates. Glob Chang Biol 14:2636–2660Google Scholar
  45. 45.
    Moore JC, Berlow EL, Coleman DC et al (2004) Detritus, trophic dynamics and biodiversity. Ecol Lett 7:584–600CrossRefGoogle Scholar
  46. 46.
    Talley SM, Coley PD, Kursar TA (2002) The effects of weather on fungal abundance and richness among 25 communities in the Intermountain West. BMC Ecol 2:1–11CrossRefGoogle Scholar
  47. 47.
    Blankinship JC, Niklaus PA, Hungate BA (2011) A meta-analysis of responses of soil biota to global change. Oecologia 165:553–565CrossRefPubMedGoogle Scholar
  48. 48.
    Morgado L, Semenova TA, Welker JM, Walker MD, Smets E, Geml JO (2015) Summer temperature increase has distinct effects on the ectomycorrhizal fungal communities of moist tussock and dry tundra in Arctic Alaska. Glob Chang Biol 21:959–972CrossRefPubMedGoogle Scholar
  49. 49.
    Allison SD, Treseder KK (2008) Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Glob Chang Biol 14:2898–2909CrossRefGoogle Scholar
  50. 50.
    Allison SD, McGuire KL, Treseder KK (2010) Resistance of microbial and soil properties to warming treatment seven years after boreal fire. Soil Biol Biochem 42:1872–1878CrossRefGoogle Scholar
  51. 51.
    Rousk J, Bååth E (2011) Growth of saprotrophic fungi and bacteria in soil. FEMS Microbiol Ecol 78:17–30CrossRefPubMedGoogle Scholar
  52. 52.
    Jaatinen K, Laiho R, Vuorenmaa A et al (2008) Microbial communities and soil respiration along a water-level gradient in a northern boreal fen. Environ Microbiol 10:339–353CrossRefPubMedGoogle Scholar
  53. 53.
    Philben M, Holmquist J, MacDonald G, Duan D, Kaiser K, Benner R (2015) Temperature, oxygen, and vegetation controls on decomposition in a James Bay peatland. Glob Biogeochem Cycles 29:729–743CrossRefGoogle Scholar
  54. 54.
    Gleason FH, Letcher PM, McGee PA (2004) Some Chytridiomycota in soil recover from drying and high temperatures. Mycol Res 108:583–589CrossRefPubMedGoogle Scholar
  55. 55.
    Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744CrossRefPubMedGoogle Scholar
  56. 56.
    Bever JD, Platt TG, Morton ER (2012) Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annu Rev Microbiol 66:265–283CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Dean SL, Warnock DD, Litvak ME, Porras-Alfaro A, Sinsabaugh R (2015) Root-associated fungal community response to drought-associated changes in vegetation community. Mycologia 107:1089–1104CrossRefPubMedGoogle Scholar
  58. 58.
    Ramos-Zapata J, Orellana R, Guadarrama P, Medina-Peralta S (2009) Contribution of mycorrhizae to early growth and phosphorus uptake by a neotropical palm. J Plant Nutr 32:855–866CrossRefGoogle Scholar
  59. 59.
    Mayerhofer MS, Kernaghan G, Harper KA (2013) The effects of fungal root endophytes on plant growth: a meta-analysis. Mycorrhiza 23:119–128CrossRefPubMedGoogle Scholar
  60. 60.
    Hribljan JA, Kane ES, Pypker TG, Chimner RA (2014) The effect of long-term water table manipulations on dissolved organic carbon dynamics in a poor fen peatland. J Geophys Res Biogeosci 119:577–595CrossRefGoogle Scholar
  61. 61.
    Kane ES, Mazzoleni LR, Kratz CJ et al (2014) Peat porewater dissolved organic carbon concentration and lability increase with warming: a field temperature manipulation experiment in a poor-fen. Biogeochemistry 119:161–178CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Department of BiologyThe University of Western OntarioLondonCanada

Personalised recommendations