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PLOS ONE  2014 

Nitrogen and Carbon Reallocation in Fungal Mycelia during Decomposition of Boreal Forest Litter

DOI: 10.1371/journal.pone.0092897

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Abstract:

Boreal forests are characterized by spatially heterogeneous soils with low N availability. The decomposition of coniferous litter in these systems is primarily performed by basidiomycete fungi, which often form large mycelia with a well-developed capacity to reallocate resources spatially- an advantageous trait in heterogeneous environments. In axenic microcosm systems we tested whether fungi increase their biomass production by reallocating N between Pinus sylvestris (Scots pine) needles at different stages of decomposition. We estimated fungal biomass production by analysing the accumulation of the fungal cell wall compound chitin. Monospecific systems were compared with systems with interspecific interactions. We found that the fungi reallocated assimilated N and mycelial growth away from well-degraded litter towards fresh litter components. This redistribution was accompanied by reduced decomposition of older litter. Interconnection of substrates increased over-all fungal C use efficiency (i.e. the allocation of assimilated C to biomass rather than respiration), presumably by enabling fungal translocation of growth-limiting N to litter with higher C quality. Fungal connection between different substrates also restricted N-mineralization and production of dissolved organic N, suggesting that litter saprotrophs in boreal forest ecosystems primarily act to redistribute rather than release N. This spatial integration of different resource qualities was hindered by interspecific interactions, in which litters of contrasting quality were colonised by two different basidiomycete species. The experiments provide a detailed picture of how resource reallocation in two decomposer fungi leads to a more efficient utilisation of spatially separated resources under N-limitation. From an ecosystem point of view, such economic fungal behaviour could potentially contribute to organic matter accumulation in the litter layers of boreal forests.

References

[1]  Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, H?gberg P, et al. (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytologist 173: 611–620. doi: 10.1111/j.1469-8137.2006.01936.x
[2]  Berg B, Hannus K, Popoff T, Theander O (1982) Changes in organic chemical components of needle litter during decomposition. Long-term decomposition in a Scots pine forest. I. Canadian Journal of Botany 60: 1310–1319. doi: 10.1139/b82-167
[3]  Boddy L (1999) Saprotrophic cord-forming fungi: meeting the challenge of heterogeneous environments. Mycologia 91: 13–32. doi: 10.2307/3761190
[4]  Lindahl BD, Olsson S (2004) Fungal translocation-creating and responding to environmental heterogeneity. Mycologist 18: 79–88. doi: 10.1017/s0269915x04002046
[5]  Tamm CO (1991) Nitrogen in Terrestrial Ecosystems-questions of productivity, vegetational changes, and ecosystem stability; Billings WD, Golley F, Lange OL, Olson JS, Remmert H, editors. Berlin: Springer-Verlag.
[6]  Berg B (2000) Litter decomposition and organic matter turnover in northern forest soils. Forest ecology and Management 133: 13–22. doi: 10.1016/s0378-1127(99)00294-7
[7]  Boberg J, Finlay RD, Stenlid J, Nasholm T, Lindahl BD (2008) Glucose and ammonium additions affect needle decomposition and carbon allocation by the litter degrading fungus Mycena epipterygia. Soil Biology & Biochemistry 40: 995–999. doi: 10.1016/j.soilbio.2007.11.005
[8]  Allison SD, LeBauer DS, Ofrecio MR, Reyes R, Ta A-M, et al. (2009) Low levels of nitrogen addition stimulate decomposition by boreal forest fungi. Soil Biology & Biochemistry 41: 293–302. doi: 10.1016/j.soilbio.2008.10.032
[9]  Boberg JB, Nasholm T, Finlay RD, Stenlid J, Lindahl BD (2011) Nitrogen availability affects saprotrophic basidiomycetes decomposing pine needles in a long term laboratory study. Fungal Ecology 4: 408–416. doi: 10.1016/j.funeco.2011.03.004
[10]  Fahey TL, Yavitt JB, Pearson JA, Knight DH (1985) The nitrogen cycle in lodgepole pine forests, souteastern Wyoming. Biogeochemistry 1: 257–275. doi: 10.1007/bf02187202
[11]  Melillo JM, Aber JD, Linkins AE, Ricca A, Fry B, et al. (1989) Carbon and nitrogen dynamics along the decay continuum - plant litter to soil organic-matter. Plant and Soil 115: 189–198. doi: 10.1007/bf02202587
[12]  Moore TR, Trofymow JA, Prescott CE, Fyles J, Titus BD (2006) Patterns of carbon, nitrogen and phosphorus dynamics in decomposing foliar litter in Canadian forests. Ecosystems 9: 46–62. doi: 10.1007/s10021-004-0026-x
[13]  Frey SD, Elliott ET, Paustian K, Peterson GA (2000) Fungal translocation as a mechanism for soil nitrogen inputs to surface residue decomposition in a no-tillage agroecosystem. Soil Biology & Biochemistry 32: 689–698. doi: 10.1016/s0038-0717(99)00205-9
[14]  Hart SC, Firestone MK (1990) Forest floor- mineral soil interactions in the internal nitrogen cycle of an old-growth forest. Biogeochemistry 12: 73–97. doi: 10.1007/bf00001809
[15]  Zeller B, Colin-Belgrand M, Dambrine E, Martin F (1998) 15N-partitioning and production of 15N-labelled litter in beech trees following [15N]urea spray. Annales Des Sciences Forestieres 55: 375–383. doi: 10.1051/forest:19980308
[16]  Lindahl B, Boberg J (2008) Distribution and function of litter basidiomycetes in coniferous forests. In: Boddy L, Frankland JC, Van West P, editors. Ecology of Saprotrophic Basidiomycetes. London: Elsevier Ltd. pp. 183–196.
[17]  Boberg J (2009) Litter decomposing fungi in boreal forests-their function in carbon and nitrogen circulation. Uppsala: Swedish University of Agricultural Sciences. 67 p.
[18]  Baldrian P, Kolarik M, Stursova M, Kopecky J, Valaskova V, et al. (2012) Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISME journal 6: 248–258. doi: 10.1038/ismej.2011.95
[19]  Boddy L (2000) Interspecific combative interactions between wood-decaying basidiomycetes. Fems Microbiology Ecology 31: 185–194. doi: 10.1111/j.1574-6941.2000.tb00683.x
[20]  Woodward S, Boddy L (2008) Interactions between saprotrophic fungi. In: Boddy L, Frankland JC, Van West P, editors. Ecology of Saprotrophic Basidiomycetes. London: Elsevier Ltd. pp. 125–141.
[21]  Frankland JC (1998) Fungal succession-unravelling the unpredictable. Mycological Research 102: 1–15. doi: 10.1017/s0953756297005364
[22]  O'Brien HE, Parrent JL, Jackson JA, Moncalvo JM, Vilgalys R (2005) Fungal community analysis by large-scale sequencing of environmental samples. Applied and Environmental Microbiology 71: 5544–5550. doi: 10.1128/aem.71.9.5544-5550.2005
[23]  Boberg JB, Ihrmark K, Lindahl BD (2011) Decomposing capacity of fungi commonly detected in Pinus sylvestris needle litter. Fungal Ecology 4: 110–114. doi: 10.1016/j.funeco.2010.09.002
[24]  Axelsson B, Br?kenhielm S (1980) Investigation sites of the Swedish coniferous forest project- biological and physiograpical features. Ecological Bulletins 32: 25–64.
[25]  Johansson M-B, Berg B, Meentemeyer V (1995) Litter mass-loss rates in late stages of decomposition in a climate transect of pine forest. Long-term decomposition in a Scots pine forest. IX. Can J Bot 73: 1509–1521. doi: 10.1139/b95-163
[26]  Ekblad A, N?sholm T (1996) Determination of chitin in fungi and mycorrhizal roots by an improved HPLC analysis of glucosamine. Plant and Soil 178: 29–35. doi: 10.1007/bf00011160
[27]  Fry B (2006) Stable Isotope Ecology. New York: Springer. 308 p.
[28]  Chadwick DR, Ineson P, Woods C, Piearce TG (1998) Decomposition of Pinus sylvestris litter in litter bags: Influence of underlying native litter layer. Soil Biology & Biochemistry 30: 47–55. doi: 10.1016/s0038-0717(97)00090-4
[29]  Berg B, Staaf H (1981) Leaching, Accumulation and Release of Nitrogen in Decomposing Forest Litter. In: Clark FE, Rosswall T, editors. Terrestrial Nitrogen Cycles. Stockholm: Swedish Natural Science research Council. pp. 163–178.
[30]  Gebauer G, Zeller B, Schimdt G, Buchmann N, Colin-Belgrand M, et al.. (2000) The fate of 15N-labelled nitrogen inputs to coniferous and broadleaf forests. In: Schulze E-D, editor. Carbon and nitrogen cycling in european forest ecosystems. Heidelberg: Springer Verlag. pp. 144–170.
[31]  Lindahl BD, Finlay RD (2006) Activities of chitinolytic enzymes during primary and secondary colonization of wood by basidiomycetous fungi. New Phytologist 169: 389–397. doi: 10.1111/j.1469-8137.2005.01581.x
[32]  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. doi: 10.1111/j.1469-8137.1989.tb00713.x
[33]  Ekschmitt K, Liu M, Vetter S, Fox O, Wolters V (2005) Strategies used by soil biota to overcome soil organic matter stability - Why is dead organic matter left over in the soil? Geoderma 128: 167–176. doi: 10.1016/j.geoderma.2004.12.024
[34]  Allison SD (2006) Brown ground: A soil carbon analogue for the green world hypothesis? American naturalist 167: 619–627. doi: 10.1086/503443
[35]  Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, et al. (2011) Persistence of soil organic matter as an ecosystem property. Nature 478: 49–56. doi: 10.1038/nature10386
[36]  Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biology & Biochemistry 32: 1485–1498. doi: 10.1016/s0038-0717(00)00084-5
[37]  Northup RR, Yu ZS, Dahlgren RA, Vogt KA (1995) Polyphenol control of nitrogen release from pine litter. Nature 377: 227–229. doi: 10.1038/377227a0
[38]  Schimel JP, Bennet J (2004) Nitrogen mineralization: Challenges of a changing paradigm. Ecology 85: 591–602. doi: 10.1890/03-8002
[39]  Boberg JB, Finlay RD, Stenlid J, Lindahl BD (2010) Fungal C translocation restricts N-mineralization in heterogeneous environments. Functional Ecology 24: 454–459. doi: 10.1111/j.1365-2435.2009.01616.x
[40]  Lindahl BO, Taylor AFS, Finlay RD (2002) Defining nutritional constrains on carbon cycling in boreal forests - towards a less ‘phytocentric’ perspective. Plant and soil 242: 123–135.
[41]  Lenoir L, Persson T, Bengtsson J, Wallander H, Wiren A (2007) Bottom-up or top-down control in forest soil microcosms? Effects of soil fauna on fungal biomass and C/N mineralisation. Biology and Fertility of Soils 43: 281–294. doi: 10.1007/s00374-006-0103-8
[42]  Piccolo A, Nardi S, Concheri G (1996) Micelle-like conformation of humic substances as revealed by size exclusion chromatography. Chemosphere 33: 595–602. doi: 10.1016/0045-6535(96)00210-x
[43]  Simpson AJ, Kingery WL, Hayes MHB, Spraul M, Humpfer E, et al. (2002) Molecular structures and associations of humic substances in the terrestrial environment. Naturwissenschaften 89: 84–88. doi: 10.1007/s00114-001-0293-8
[44]  Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, et al. (2013) Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339: 1615–1618. doi: 10.1126/science.1231923
[45]  Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrint cycling in ecosystems- a journey toward relevance. New Phytologist 157: 475–492. doi: 10.1046/j.1469-8137.2003.00704.x
[46]  Newell K (1984) Interaction between two decomposer basidiomycetes and a collembolan under sitka spruce -grazing and its potential effects on fungal distribution and litter decomposition Soil Biology & Biochemistry. 16: 235–239. doi: 10.1016/0038-0717(84)90007-5
[47]  Robinson CH, Dighton J, Frankland JC, Coward PA (1993) Nutrient and carbon dioxide release by interacting species of straw-decomposing fungi. Plant and Soil 151: 139–142. doi: 10.1007/bf00010794
[48]  van der Wal A, Geydan TD, Kuyper TW, de Boer W (2013) A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes. FEMS Microbiology Reviews 37: 477–494. doi: 10.1111/1574-6976.12001
[49]  Appuhn A, Joergensen RG (2006) Microbial colonisation of roots as a function of plant species. Soil Biology & Biochemistry 38: 1040–1051. doi: 10.1016/j.soilbio.2005.09.002
[50]  Frankland JC, Lindley DK, Swift MJ (1978) A comparison of two methods for estimation of mycelial biomass in leaf litter Soil Biology & Biochemistry. 10: 323–333. doi: 10.1016/0038-0717(78)90030-5
[51]  Paul EA (2007) Soil microbiology, ecology and biochemistry. Canada: Academic Press. 532 p.
[52]  Boddy L, Watkinson SC (1995) Wood decomposition, higher fungi, and their role in nutrient redistribution. Canadian Journal of Botany 73: S1377–S1383. doi: 10.1139/b95-400
[53]  Wallander H, Nilsson LO, Hagerberg D, Rosengren U (2003) Direct estimates of C:N ratios of ectomycorrhizal mycelia collected from Norway spruce forest soils. Soil Biology & Biochemistry 35: 997–999. doi: 10.1016/s0038-0717(03)00121-4
[54]  Levi MP, Cowling EB (1969) Role of nitrogen in wood deterioration. VII. Physiological adaption of wood-destroying and other fungi to substrate deficient nitrogen. Phytopathology 59: 460–468.
[55]  Venables CE, Watkinson SC (1989) Medium-induced changes in patterns of free and combined amino-acids in mycelium of Serpula lacrymans. Mycological Research 92: 273–277. doi: 10.1016/s0953-7562(89)80065-6

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