Changes in fungal communities along a boreal forest soil fertility gradient

New Phytologist

Volumn 207, Issue 4, 2015, Pages 1145-1158

  Sterkenburg, Erica ^a   Bahr, Adam ^b   Brandström Durling, Mikael ^a   Clemmensen, Karina E ^a   Lindahl, Björn D ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b LUND UNIVERSITY   (Sweden)

Author keywords

Ecosystem fertility; Ergosterol; Fungal biomass; Fungal communities; High throughput sequencing; Mycorrhiza

Indexed keywords

BIOMASS ALLOCATION; BOREAL FOREST; DOMINANCE; FOREST SOIL; FUNCTIONAL GROUP; FUNGUS; GROWTH RESPONSE; OLD-GROWTH FOREST; RELATIVE ABUNDANCE; SOIL FERTILITY;

SWEDEN;

ASCOMYCOTA; BASIDIOMYCOTA; FUNGI; PICEA ABIES; PINUS SYLVESTRIS;

CARBON; ERGOSTEROL; NITROGEN; SOIL;

CHEMISTRY; DNA SEQUENCE; FERTILITY; FUNGUS; METABOLISM; MICROBIOLOGY; PH; PHYSIOLOGY; PLANT LEAF; SOIL; SPECIES DIFFERENCE; STATISTICAL MODEL; TAIGA; TREE;

CARBON; ERGOSTEROL; FERTILITY; FUNGI; HYDROGEN-ION CONCENTRATION; LINEAR MODELS; NITROGEN; PLANT LEAVES; SEQUENCE ANALYSIS, DNA; SOIL; SOIL MICROBIOLOGY; SPECIES SPECIFICITY; TAIGA; TREES;

EID: 84938416454     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13426     Document Type: Article

References (54)

1. Abarenkov K, Tedersoo L, Nilsson RH, Vellak K, Saar I, Veldre V, Parmasto E, Prous M, Aan A, Ots M et al. 2010. PlutoF - a web based workbench for ecological and taxonomic research, with an online implementation for fungal ITS sequences. Evolutionary Bioinformatics 6: 189-196.
2. Aerts R. 1995. The advantages of being evergreen. Trends in Ecology and Evolution 10: 402-407.
3. 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.
4. Berg B. 2000. Litter decomposition and organic matter turnover in northern forest soils. Forest Ecology and Management 133: 13-22.
5. Boberg JB, Finlay RD, Stenlid J, Ekblad A, Lindahl BD. 2014. Nitrogen and carbon reallocation in fungal mycelia during decomposition of boreal forest litter. PLoS One 9: e92897.
6. Boberg J, Finlay RD, Stenlid J, Näsholm T, Lindahl BD. 2008. Glucose and ammonium additions affect needle decomposition and carbon allocation by the litter degrading fungs Mycena epipterygia. Soil Biology and Biochemistry 40: 995-999.
7. Boberg JB, Ihrmark K, Lindahl BD. 2011. Decomposing capacity of fungi commonly detected in Pinus sylvestris needle litter. Fungal Ecology 4: 110-114.
8. Boddy L. 2000. Interspecific combative interactions between wood-decaying basidiomycetes. FEMS Microbiology Ecology 31: 185-194.
9. Bödeker ITM, Clemmensen KE, de Boer W, Martin F, Olson Å, Lindahl BD. 2014. Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems. New Phytologist 203: 245-256.
10. Butenschoen O, Poll C, Langel R, Kandeler E, Marhan S, Scheu S. 2007. Endogeic earthworms alter carbon translocation by fungi at the soil-litter interface. Soil Biology and Biochemistry 39: 2854-2864.
11. 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.
12. Clemmensen KE, Finlay RD, Dahlberg A, Stenlid J, Wardle DA, Lindahl BD. 2015. Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests. New Phytologist 205: 1525-1536.
13. Clemmensen KE, Michelsen A, Jonasson S, Shaver GR. 2006. Increased ectomycorrhizal fungal abundance after long-term fertilization and warming of two arctic tundra ecosystems. New Phytologist 171: 391-404.
14. Cooke RC, Rayner ADM. 1984. Ecology of saprotrophic fungi. London, UK & New York, NY, USA: Longman.
15. Crowther TW, Maynard DS, Crowther TR, Peccia J, Smith JR, Bradford MA. 2014. Untangling the fungal niche: the trait-based approach. Frontiers in Microbiology 5: 579.
16. Crowther TW, Stanton DWG, Thomas SM, A'Bear DA, Hiscox J, Jones TH, Voriskova J, Baldrian P, Boddy L. 2013. Top-down control of soil fungal community composition by a globally distributed keystone consumer. Ecology 94: 2518-2528.
17. Ekblad A, Wallander H, Godbold DL, Cruz C, Johnson D, Baldrian P, Björk 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.
18. Fernandez CW, Koide RT. 2014. Initial melanin and nitrogen concentrations control the decomposition of ectomycorrhizal fungal litter. Soil Biology & Biochemistry 77: 150-157.
19. Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martinez AT, Otillar R, Spatafora JW, Yadav JS et al. 2012. The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336: 1715-1719.
20. Frank DN. 2009. BARCRAWL and BARTAB: software for design and implementation of barcoded primers for highly multiplexed DNA sequencing. BMC Bioinformatics 10: 362.
21. Gostinčar C, Grube M, De Hoog S, Zalar P, Gunde-Cimerman N. 2010. Extremotolerance in fungi: evolution on the edge. FEMS Microbiology Ecology 71: 2-11.
22. Grime JP. 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. The American Naturalist 111: 1169-1194.
23. Haimi J, Einbork M. 1992. Effects of endogenic earthworms on soil processes and plant-growth in coniferous forest soil. Biology and Fertility of Soils 13: 6-10.
24. Högberg MN, Bååth E, Nordgren A, Arnebrant K, Högberg P. 2003. Contrasting effects of nitrogen availability on plant carbon supply to mycorrhizal fungi and saprotrophs - a hypothesis based on field observations in boreal forest. New Phytologist 160: 225-238.
25. Högberg MN, Briones MJI, Keel SG, Metcalfe DB, Campbell C, Midwood AJ, Thornton B, Hurry V, Linder S, Nasholm T et al. 2010. Quantification of effects of season and nitrogen supply on tree below-ground carbon transfer to ectomycorrhizal fungi and other soil organisms in a boreal pine forest. New Phytologist 187: 485-493.
26. Högberg MN, Högberg P, Myrold DD. 2006. Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three? Oecologia 150: 590-601.
27. Högberg P, Johannisson C, Yarwood S, Callesen I, Näsholm T, Myrold DD, Hogberg MN. 2011. Recovery of ectomycorrhiza after 'nitrogen saturation' of a conifer forest. New Phytologist 189: 515-525.
28. Ihrmark K, Bödeker ITM, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, Strid Y, Stenlid J, Brandstrom-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.
29. Janssens IA, Dieleman W, Luyssaert S, Subke JA, Reichstein M, Ceulemans R, Ciais P, Dolman AJ, Grace J, Matteucci G et al. 2010. Reduction of forest soil respiration in response to nitrogen deposition. Nature Geoscience 3: 315-322.
30. Kalliokoski T, Pennanen T, Nygren P, Sievänen R, Helmisaari H-S. 2010. Belowground interspecific competition in mixed boreal forests: fine root and ectomycorrhiza characteristics along stand developmental stage and soil fertility gradients. Plant and Soil 330: 73-89.
31. Kjøller R, Nilsson LO, Hansen K, Schmidt IK, Vesterdal L, Gundersen P. 2012. Dramatic changes in ectomycorrhizal community composition, root tip abundance and mycelial production along a stand-scale nitrogen deposition gradient. New Phytologist 194: 278-286.
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. Koide R, Fernandez C, Petprakob K. 2011. General principles in the community ecology of ectomycorrhizal fungi. Annals of Forest Science 68: 45-55.
34. Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM et al. 2013. Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology 22: 5271-5277.
35. Lahti T, Väisänen R. 1987. Ecological gradients of boreal forests in South Finland: an ordination test of Cajander's forest site type theory. Vegetatio 68: 145-156.
36. Lilleskov EA, Fahey TJ, Horton TR, Lovett GM. 2002. Belowground ectomycotthizal fungal community change over anitrogen deposition gradient in Alaska. Ecology 83: 104-115.
37. Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay RD. 2007. Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytologist 173: 611-620.
38. Lindahl BD, Nilsson RH, Tedersoo L, Abarenkov K, Carlsen T, Kjøller R, Koljalg U, Pennanen T, Rosendahl S, Stenlid J et al. 2013. Fungal community analysis by high-throughput sequencing of amplified markers - a user's guide. New Phytologist 199: 288-299.
39. Lindahl BD, Olsson S. 2004. Fungal translocation - creating and responding to environmental heterogeneity. New Phytologist 18: 79-88.
40. Matheny PB, Curtis JM, Hofstetter V, Aime MC, Moncalvo JM, Ge ZW, Yang ZL, Slot JC, Ammirati JF, Baroni TJ et al. 2006. Major clades of Agaricales: a multilocus phylogenetic overview. Mycologia 98: 982-995.
41. Moorhead DL, Sinsabaugh RL. 2006. A theoretical model of litter decay and microbial interaction. Ecological Monographs 76: 151-174.
42. Nguyen NH, Smith D, Kabir P, Kennedy P. 2015. Parsing ecological signal from noise in next generation amplicon sequencing. New Phytologist 205: 1389-1393.
43. Nilsson LO, Bååth E, Falkengren-Grerup U, Wallander H. 2007. Growth of ectomycorrhizal mycelia and composition of soil microbial communities in oak forest soils along a nitrogen deposition gradient. Oecologia 153: 375-384.
44. Nilsson LO, Wallander H. 2003. Production of external mycelium by ectomycorrhizal fungi in a Norway spruce forest was reduced in response to nitrogen fertilization. New Phytologist 158: 409-416.
45. Nylund JE, Wallander H. 1992. Ergosterol analysis as a means of quantifying mycorrhizal biomass. Methods in Microbiology 24: 77-88.
46. Pennanen T, Liski J, Bååth E, Kitunen V, Uotila J, Westman CJ, Fritze H. 1999. Structure of the microbial communities in coniferous forest soils in relation to site fertility and stand development stage. Microbial Ecology 38: 168-179.
47. Read DJ, Perez-Moreno J. 2003. Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? New Phytologist 157: 475-492.
48. Rosling A, Cox F, Cruz-Martinez K, Ihrmark K, Grelet GA, Lindahl BD, Menkis A, James TY. 2011. Archaeorhizomycetes: unearthing an ancient class of ubiquitous soil fungi. Science 333: 876-879.
49. Swedish Forest Soil Survey. [WWW document] URL http://www.slu.se/markinventeringen. [accessed 10 December 2014].
50. Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yorou NS, Wijesundera R, Villarreal Ruiz L, Vasco-Palacios AM, Quang Tedersoo L, Bahram M et al. 2014. Global diversity and geography of soil fungi. Science 346: 1078.
51. Vitousek PM, Howarth RW. 1991. Nitrogen limitation on land and in the sea- how can it occur. Biogeochemistry 13: 87-115.
52. Vrålstad T, Myhre E, Schumacher T. 2002. Molecular diversity and phylogenetic affinities of symbiotic root-associated ascomycetes of the Helotiales in burnt and metal polluted habitats. New Phytologist 155: 131-148.
53. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M et al. 2004. The worldwide leaf economics spectrum. Nature 428: 821-827.
54. Zhao J, Zeng J, de Hoog GS, Attili-Angelis D, Prenafeta-Boldú FX. 2010. Isolation and identification of black yeasts by enrichment on atmospheres of monoaromatic hydrocarbons. Microbial Ecology 60: 149-156.