Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests

New Phytologist

Volumn 205, Issue 4, 2015, Pages 1525-1536

  Clemmensen, Karina E ^a   Finlay, Roger D ^a   Dahlberg, Anders ^a   Stenlid, Jan ^a   Wardle, David A ^a   Lindahl, Björn D ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

454 sequencing; Betula pubescens; Boreal forest; Carbon (C) sequestration; Ectomycorrhizal exploration types; Mycorrhizal symbiosis; Picea abies; Pinus sylvestris

Indexed keywords

BIOMASS; BOREAL FOREST; CARBON SEQUESTRATION; CHRONOSEQUENCE; COMMUNITY STRUCTURE; CONIFEROUS TREE; DECIDUOUS TREE; ECTOMYCORRHIZA; FOREST SOIL; FUNGUS; SOIL CARBON; SOIL NITROGEN; SOIL PROFILE; SUCCESSION;

ASCOMYCOTA; BETULA PUBESCENS; CORTINARIUS; FUNGI; PICEA ABIES; PINUS SYLVESTRIS; SUILLUS;

BIODIVERSITY; BIOLOGICAL MODEL; CARBON SEQUESTRATION; ECOSYSTEM; ISLAND (GEOLOGICAL); MYCORRHIZA; PHYLOGENY; PHYSIOLOGY; SPECIES DIFFERENCE; SWEDEN; TAIGA; TIME;

BIODIVERSITY; CARBON SEQUESTRATION; ECOSYSTEM; ISLANDS; MODELS, BIOLOGICAL; MYCORRHIZAE; PHYLOGENY; SPECIES SPECIFICITY; SWEDEN; TAIGA; TIME FACTORS;

EID: 84922809677     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13208     Document Type: Article

References (55)

1. Abarenkov K, Nilsson RH, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Hoiland K, Kjoller R, Larsson E, Pennanen T et al. 2010. The UNITE database for molecular identification of fungi - recent updates and future perspectives. New Phytologist 186: 281-285.
2. Abuzinadah RA, Finlay RD, Read DJ. 1986. The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. 2. Utilization of protein by mycorrhizal plants of Pinus contorta. New Phytologist 103: 495-506.
3. Agerer R. 2006. Fungal relationships and structural identity of their ectomycorrhizae. Mycological Progress 5: 67-107.
4. 2. Plant and Soil 296: 159-172.
5. Averill C, Turner BL, Finzi AC. 2014. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505: 543-545.
6. Baldrian P, Kolarik M, Stursova M, Kopecky J, Valaskova V, Vetrovsky T, Zifcakova L, Snajdr J, Ridl J, Vlcek C et al. 2012. Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. Isme Journal 6: 248-258.
7. Baldrian P, Vetrovsky T, Cajthaml T, Dobiasova P, Petrankova M, Snajdr J, Eichlerova I. 2013. Estimation of fungal biomass in forest litter and soil. Fungal Ecology 6: 1-11.
8. Boddy L. 1999. Saprotrophic cord-forming fungi: meeting the challenge of heterogeneous environments. Mycologia 91: 13-32.
9. Bödeker ITM, Clemmensen KE, de Boer W, Martin F, Olson A, Lindahl BD. 2014. Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems. New Phytologist 203: 245-256.
10. Brovkin V, van Bodegom PM, Kleinen T, Wirth C, Cornwell WK, Cornelissen JHC, Kattge J. 2012. Plant-driven variation in decomposition rates improves projections of global litter stock distribution. Biogeosciences 9: 565-576.
11. Butler MJ, Day AW. 1998. Fungal melanins: a review. Canadian Journal of Microbiology 44: 1115-1136.
12. Cairney JWG. 2012. Extramatrical mycelia of ectomycorrhizal fungi as moderators of carbon dynamics in forest soil. Soil Biology & Biochemistry 47: 198-208.
13. Chen J. 2012. GUniFrac: generalized UniFrac distances. R package version 1.0. [WWW document] URL http://CRAN.R-project.org/package=GUniFrac [accessed 14 June 2013].
14. 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.
15. Coelho RRR, Sacramento DR, Linhares LF. 1997. Amino sugars in fungal melanins and soil humic acids. European Journal of Soil Science 48: 425-429.
16. Dowson CG, Springham P, Rayner ADM, Boddy L. 1989. Resource relationships of foraging mycelial systems of Phanerochaete velutina and Hypholoma fasciculare in soil. New Phytologist 111: 501-509.
17. 2. Ecology Letters 14: 349-357.
18. Drigo B, Anderson IC, Kannangara GSK, Cairney JWG, Johnson D. 2012. Rapid incorporation of carbon from ectomycorrhizal mycelial necromass into soil fungal communities. Soil Biology & Biochemistry 49: 4-10.
19. Ekblad A, Wallander H, Godbold DL, Cruz C, Johnson D, Baldrian P, Bjork RG, Epron D, Kieliszewska-Rokicka B, Kjoller R et al. 2013. The production and turnover of extramatrical mycelium of ectomycorrhizal fungi in forest soils: role in carbon cycling. Plant and Soil 366: 1-27.
20. Falconer RE, Bown JL, White NA, Crawford JW. 2007. Biomass recycling: a key to efficient foraging by fungal colonies. Oikos 116: 1558-1568.
21. Fernandez CW, Koide RT. 2012. The role of chitin in the decomposition of ectomycorrhizal fungal litter. Ecology 93: 24-28.
22. Fernandez CW, Koide RT. 2013. The function of melanin in the ectomycorrhizal fungus Cenococcum geophilum under water stress. Fungal Ecology 6: 479-486.
23. Fernandez CW, Koide RT. 2014. Initial melanin and nitrogen concentrations control the decomposition of ectomycorrhizal fungal litter. Soil Biology & Biochemistry 77: 150-157.
24. 14C-labelled carbon between plants interconnected by a common mycelium. New Phytologist 103: 143-156.
25. Gadgil RL, Gadgil PD. 1971. Mycorrhiza and litter decomposition. Nature 233: 133.
26. Grelet GA, Johnson D, Vralstad T, Alexander IJ, Anderson IC. 2010. New insights into the mycorrhizal Rhizoscyphus ericae aggregate: spatial structure and co-colonization of ectomycorrhizal and ericoid roots. New Phytologist 188: 210-222.
27. Hobbie EA. 2006. Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology 87: 563-569.
28. Hobbie EA, Agerer R. 2010. Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types. Plant and Soil 327: 71-83.
29. Hobbie EA, Ouimette AP, Schuur EAG, Kierstead D, Trappe JM, Bendiksen K, Ohenoja E. 2013. Radiocarbon evidence for the mining of organic nitrogen from soil by mycorrhizal fungi. Biogeochemistry 114: 381-389.
30. Ihrmark K, Bödeker I, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, Strid Y, Stenlid J, Brandström-Durling M, Clemmensen KE et al. 2012. New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiology Ecology 82: 666-677.
31. Kerley SJ, Read DJ. 1998. 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 Phytologist 139: 353-360.
32. Koide RT, Fernandez C, Malcolm G. 2013. Determining place and process: functional traits of ectomycorrhizal fungi that affect both community structure and ecosystem function. New Phytologist 201: 433-439.
33. Langley JA, Hungate BA. 2003. Mycorrhizal controls on belowground litter quality. Ecology 84: 2302-2312.
34. Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Hogberg P, Stenlid J, Finlay RD. 2007. Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytologist 173: 611-620.
35. Lindahl BD, Tunlid A. in press. Ectomycorrhizal fungi - potential organic matter decomposers, yet not saprotrophs. New Phytologist. doi: 10.1111/nph.13201.
36. Makkonen M, Berg MP, Handa IT, Hattenschwiler S, van Ruijven J, van Bodegom PM, Aerts R. 2012. Highly consistent effects of plant litter identity and functional traits on decomposition across a latitudinal gradient. Ecology Letters 15: 1033-1041.
37. McGuire KL, Allison SD, Fierer N, Treseder KK. 2013. Ectomycorrhizal-dominated boreal and tropical forests have distinct fungal communities, but analogous spatial patterns across soil horizons. PLoS ONE 8: e68278.
38. Näsholm T, Högberg P, Franklin O, Metcalfe D, Keel SG, Campbell C, Hurry V, Linder S, Högberg MN. 2013. Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests? New Phytologist 198: 214-221.
39. Oksanen J, Kindt R, Legendre P, O'Hara B, Stevens MHH, Oksanen MJ, Suggests M. 2007. Vegan: community ecology package. [WWW document] URL http://vegan.r-forge.r-project.org/ [accessed 14 June 2013].
40. Pan YD, Birdsey RA, Fang JY, Houghton R, Kauppi PE, Kurz WA, Phillips OL, Shvidenko A, Lewis SL, Canadell JG et al. 2011. A large and persistent carbon sink in the world's forests. Science 333: 988-993.
41. 2. Ecology Letters 15: 1042-1049.
42. 2-enrichment. Global Change Biology 14: 1252-1264.
43. R Core Team. 2013. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. [WWW document] URL http://www.R-project.org/ [accessed 14 June 2013].
44. Read DJ, Leake JR, Perez-Moreno J. 2004. Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Canadian Journal of Botany 82: 1243-1263.
45. Robinson CH. 2001. Cold adaptation in Arctic and Antarctic fungi. New Phytologist 151: 341-353.
46. Russell AE. 2014. Unexpected effects of chitin, cellulose, and lignin addition on soil dynamics in a wet tropical forest. Ecosystems 17: 918-930.
47. Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. Cambridge, UK: Academic Press.
48. Tedersoo L, Smith ME. 2013. Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biology Reviews 27: 83-99.
49. Treseder KK, Allen MF, Ruess RW, Pregitzer KS, Hendrick RL. 2005. Lifespans of fungal rhizomorphs under nitrogen fertilization in a pinyon-juniper woodland. Plant and Soil 270: 249-255.
50. Vohnik M, Albrechtova J. 2011. The co-occurrence and morphological continuum between ericoid mycorrhiza and dark septate endophytes in roots of six European rhododendron species. Folia Geobotanica 46: 373-386.
51. Vohnik M, Fendrych M, Albrechtova J, Vosatka M. 2007. Intracellular colonization of Rhododendron and Vaccinium roots by Cenococcum geophilum, Geomyces pannorum and Meliniomyces variabilis. Folia Microbiologica 52: 407-414.
52. Wallander H, Ekblad A, Godbold DL, Johnson D, Bahr A, Baldrian P, Bjork RG, Kieliszewska-Rokicka B, Kjoller R, Kraigher H et al. 2013. Evaluation of methods to estimate production, biomass and turnover of ectomycorrhizal mycelium in forests soils - a review. Soil Biology & Biochemistry 57: 1034-1047.
53. Wardle DA, Hornberg G, Zackrisson O, Kalela-Brundin M, Coomes DA. 2003. Long-term effects of wildfire on ecosystem properties across an island area gradient. Science 300: 972-975.
54. Wardle DA, Jonsson M, Bansal S, Bardgett RD, Gundale MJ, Metcalfe DB. 2012a. Linking vegetation change, carbon sequestration and biodiversity: insights from island ecosystems in a long-term natural experiment. Journal of Ecology 100: 16-30.
55. Wardle DA, Jonsson M, Kalela-Brundin M, Lagerström A, Bardgett RD, Yeates GW, Nilsson MC. 2012b. Drivers of inter-year variability of plant production and decomposers across contrasting island ecosystems. Ecology 93: 521-531.