Elevated CO 2 impacts ectomycorrhiza-mediated forest soil carbon flow: Fungal biomass production, respiration and exudation

Fungal Ecology

Volumn 5, Issue 1, 2012, Pages 85-98

  Fransson, Petra ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

Biomass; Carbon cycling; Ectomycorrhiza; Elevated CO 2; Exudation; Forest; Global change; Microbial communities; Soil respiration

Indexed keywords

FUNGI;

EID: 84155160619     PISSN: 17545048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.funeco.2011.10.001     Document Type: Article

References (127)

1. Agerer R. Exploration types of ectomycorrhizae. A proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 2001, 11:107-114.
2. Alberton O., Kuyper T.W. Ectomycorrhizal fungi associated with Pinus sylvestris seedlings respond differently to increased carbon and nitrogen availability: implications for ecosystem responses to global change. Global Change Biology 2009, 15:166-175.
3. 2. New Phytologist 2005, 167:859-868.
4. 2. Plant and Soil 2007, 296:159-172.
5. Andersen C.P., Nikolov I., Nikolova P., Matyssek R., Häberle K.-H. Estimating 'autotrophic' belowground respiration in spruce and beech forests: decreases following girdling. European Journal of Forest Research 2005, 124:155-163.
6. 3. Ecology Letters 2009, 12:813-822.
7. Antkowiak R., Antkowiak W.Z., Banczyk I., Mikolajczyk L. A new phenolic metabolite, involutone, isolated from the mushroom Paxillus involutus. Canadian Journal of Chemistry 2003, 81:118-124.
8. 2 enrichment. Global Change Biology 2010, 16:2830-2843.
9. 2 enrichment (FACE) on soil respiration. Biogeochemistry 2006, 77:91-116.
10. 2: simultaneous positive and negative below-ground feedbacks. Global Change Biology 1997, 3:247-258.
11. Bhupinderpal-Singh, Nordgren A., Löfvenius M.O., Högberg M.N., Mellander P.E., Högberg P. Tree root and soil heterotrophic respiration as revealed by girdling of boreal Scots pine forest: extending observations beyond the first year. Plant Cell and Environment 2003, 26:1287-1296.
12. 2 enrichment experiments. Global Change Biology 2010, 16:836-848.
13. 2 leads to loss of soil carbon. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:4990-4995.
14. Cheng W., Gershenson A. Carbon fluxes in the rhizosphere. The Rhizosphere - an ecological perspective 2007, 31-56. Academic Press, San Diego, CA. Z.G. Cardon, J.L. Whitbeck (Eds.).
15. 2 and mycorrhizae on nitrogen acquisition: contrasting responses in Pinus taeda and Liquidambar styraciflua. Tree Physiology 2001, 21:83-91.
16. Cudlin P., Kieliszewska-Rokicka B., Rudawska M., Grebenc T., Alberton O., Lehto T., Bakker M.R., Børja I., Konôpka B., Leski T., Kraigher H., Kuyper T.W. Fine roots and ectomycorrhizas as indicators of environmental change. Plant Biosystems 2007, 141:406-425.
17. Dakora F.D., Phillips D.A. Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant and Soil 2002, 245:35-47.
18. Dahlberg A., Croneborg H., Hallingbäck T. Sveriges ektomykorrhizasvampar - en översikt av arter, förekomst och ekologi. Svensk botanisk tidskrift 2000, 94:267-285.
19. Deacon J.W., Fleming L.V. Interactions of ectomycorrhizal fungi. Mycorrhizal Functioning 1992, 249-300. Chapman & Hall, New York, US. M. Allen (Ed.).
20. 2: a meta-analysis. Global Change Biology 2006, 12:2077-2091.
21. De Graaff M.-A., Classen A.T., Castro H.F., Schadt C.W. Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates. New Phytologist 2010, 188:1055-1064.
22. 2 and temperature. Annals of Botany 1997, 79:111-120.
23. 2. Ecology Letters 2011, 14:349-357.
24. 2 on microbial community structure and activities in the rhizosphere. Biology and Fertility of Soils 2008, 44:667-679.
25. Eilers K.G., Lauber C.L., Knight R., Fierer N. Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil. Soil Biology and Biochemistry 2010, 42:896-903.
26. 2 and N fertilization in the duke forest. Global Change Biology 2010, 16:2104-2116.
27. 2. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:14014-14019.
28. Finzi A.C., Sinsabaugh R.L., Long T.M., Osgood M.P. Microbial community responses to atmospheric carbon dioxide enrichment in a warm-temperate forest. Ecosystems 2006, 9:215-226.
29. Fransson P.M.A., Anderson I.C., Alexander I.J. Ectomycorrhizal fungal isolates respond differently to increased carbon availability. FEMS Microbiology Ecology 2007, 61:246-257.
30. 2 vary with fungal species?. Plant and Soil 2007, 291:323-333.
31. 2 and nitrogen influence exudation of soluble organic compounds by ectomycorrhizal root systems. FEMS Microbiology Ecology 2010, 71:186-196.
32. Fransson P.M.A., Taylor A.F.S., Finlay R.D. Effects of continuous optimal fertilisation upon a Norway spruce ectomycorrhizal community. Tree Physiology 2000, 20:599-606.
33. 2 alters root symbiont community structure in forest trees. New Phytologist 2001, 152:431-442.
34. 2. Mycorrhiza 2005, 15:25-31.
35. 2 and nitrogen fertilization in a warm temperate forest. Plant and Soil 2008, 303:301-310.
36. 2 concentration changes ectomycorrhizal morphotype assemblages in Betula papyrifera. Tree Physiology 1997, 17:347-350.
37. 2. New Phytologist 1997, 137:433-440.
38. Godbold D.L., Hoosbeek M.R., Lukac M., Cotrufo M.F., Janssens I.A., Ceulemans R., Polle A., Velthorst E.J., Scarascia-Mugnozza G., De Angelis P., Miglietta F., Peressotti A. Mycorrhizal hyphal turnover as a dominant process for carbon input into soil organic matter. Plant and Soil 2006, 281:15-24.
39. 2. New Phytologist 2000, 146:163-168.
40. Grayston S.J., Vaughan D., Jones D. Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Applied Soil Ecology 1996, 5:29-56.
41. 2 flux: uncovering the contribution and environmental responses of ectomycorrhizas. Global Change Biology 2007, 13:1786-1797.
42. 2 fluxes and individual mycorrhizosphere components to photosynthesis. Biogeosciences Discussions 2011, 8:3155-3201.
43. Heinonsalo J., Pumpanen J., Rasilo T., Hurme K.-R., Ilvesniemi H. Carbon partitioning in ectomycorrhizal Scots pine seedlings. Soil Biology and Biochemistry 2010, 42:1614-1623.
44. Hobbie E.A., Agerer R. Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types. Plant and Soil 2010, 327:71-83.
45. Hofmockel K.S., Schlesinger W.H. Carbon dioxide effects on heterotrophic dinitrogen fixation in a temperate pine forest. Soil Science Society of America Journal 2007, 71:140-144.
46. Holmström S.J.M., Lundström U.S., Finlay R.D., van Hees P.A.W. Siderophores in forest soil solution. Biogeochemistry 2004, 71:247-258.
47. 2 enrichment (FACE): final results of POP-EuroFACE compared to other forest FACE experiments. Ecosystems 2009, 12:220-239.
48. Högberg P., Högberg M.N. Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytologist 2002, 154:791-795.
49. Ineichen K., Wiemken V., Wiemken A. Shoots, roots and ectomycorrhiza formation of Pine-seedlings at elevated atmospheric carbon-dioxide. Plant, Cell and Environment 1995, 18:703-707.
50. 2 concentration in forested ecosystems. New Phytologist 2010, 186:346-357.
51. 2 fluxes after a decade of carbon dioxide enrichment in a warm temperate forest. Ecology 2009, 90:3352-3366.
52. Janssens I.A., Lankreijer H., Matteucci G., Kowalski A.S., Buchmann N., Epron D., Pilegaard K., Kutsch W., Longdoz B., Gruenwald T., Montagnani L., Dore S., Rebmann C., Moors E.J., Grelle A., Rannik U.E., Morgenstern K., Oltchev S., Celemnt R., Mundsson G.U., Minerbi S., Berbigier P., Ibrom A., Moncrieff J., Aubinet M., Bernhofer C., Jensen N.O., Vesala T., Granier A., Schulze E.-D., Lindroth A., Dolman A.J., Jarvis P.G., Ceulemans R., Valentini R. Productivity overshadows temperature in determining soil and ecosystem respiration across European forests. Global Change Biology 2001, 7:269-278.
53. 2 alters soil microbial communities associated with trembling aspen (Populus tremuloides) roots. Microbial Ecology 2005, 50:102-109.
54. Jastrow J.D., Miller R.M., Matamala R., Norby R.J., Boutton T.W., Rice C.W., Owensby C.E. Elevated atmospheric carbon dioxide increases soil carbon. Global Change Biology 2005, 11:2057-2064.
55. Johansson E.M., Fransson P.M.A., Finlay R.D., van Hees P.A.W. Quantitative analysis of root and ectomycorrhizal exudates as a response to Pb, Cd and As stress. Plant and Soil 2008, 313:39-54.
56. 2. Soil Biology and Biochemistry 2009, 41:1111-1116.
57. Jones D.L., Darrah P.R. Role of root derived organic acids in the mobilization of simple C substrates. Plant and Soil 1994, 166:247-257.
58. Jones D.L., Hodge A., Kuzyakov Y. Plant and mycorrhizal regulation of rhizodeposition. New Phytologist 2004, 163:459-480.
59. Kaiser C., Koranda M., Kitzler B., Fuchslueger L., Schnecker J., Schweiger P., Rasche F., Zechmeister-Boltenstern S., Sessitsch A., Richter A. Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil. New Phytologist 2010, 187:843-858.
60. 3 on roots and mycorrhizas of naturally growing young Scots pine trees during three exposure years. Global Change Biology 1999, 5:771-780.
61. 3 levels during three growing seasons. Global Change Biology 2005, 11:1167-1179.
62. 2 from four forest FACE experiments. Global Change Biology 2004, 10:1027-1042.
63. 2 on the fungal community in a coastal scrub oak forest soil investigated with terminal-restriction fragment length polymorphism analysis. Applied and Environmental Microbiology 2002, 68:4370-4376.
64. Kõljalg U., Tammi H., Timonen S., Agerer R., Sen R. ITS rDNA sequence-based phylogenetic analysis of Tomentellopsis species from boreal and temperate forests, and the identification of pink-type ectomycorrhizas. Mycological Progress 2002, 1:81-92.
65. 2 does not ameliorate effects of ozone on carbon allocation in Pinus halepensis and Betula pendula in symbiosis with Paxillus involutus. Physiologia Plantarum 1999, 106:370-377.
66. 2. Ecosystems 2003, 6:424-430.
67. Larson J.L., Zak D.R., Sinsabaugh R.L. Extracellular enzyme activity beneath temperate trees growing under elevated carbon dioxide and ozone. Soil Science Society of America Journal 2002, 66:1848-1856.
68. Lavigne M.B., Ryan M.G., Anderson D.E., Baldocchi D.D., Crill P.M., Fitzjarrald D.R., Goulden M.L., Gower S.T., Massheder J.M., McCaughey J.H., Rayment M., Striegl R.G. Comparing nocturnal eddy covariance measurements to estimates of ecosystem respiration made by scaling chamber measurements at six coniferous boreal sites. Journal of Geophysical Research-Atmospheres 1997, 102:28977-28985.
69. 2 affects soil microbial diversity associated with trembling aspen. Environmental Microbiology 2008, 10:926-941.
70. 2 on mycorrhizal colonization of Loblolly Pine (Pinus taeda L.) seedlings. Plant and Soil 1994, 165:81-88.
71. Leyval C., Berthelin J. Rhizodeposition and net release of soluble organic compounds by pine and beech seedlings inoculated with rhizobacteria and ectomycorrhizal fungi. Biology and Fertility of Soils 1993, 15:259-267.
72. 2 enrichment. Global Change Biology 2008, 14:2910-2922.
73. 2 both increase the capacity for sucrose synthesis in source leaves of spruce and aspen. New Phytologist 2000, 145:565-574.
74. 2 (POPFACE). Global Change Biology 2003, 9:838-848.
75. 2 - a case of increased throughput?. Forestry 2009, 82:75-86.
76. 2 enrichment. 1. Ectomycorrhizal fungi and soil fauna. Environmental Pollution 1996, 94:309-316.
77. 2 on fine root production and activity in an intact temperate forest ecosystem. Global Change Biology 2000, 6:967-979.
78. 2 in a model regenerating longleaf pine-wiregrass ecosystem. Ecosystems 2010, 13:901-916.
79. 2 enrichment. Tree Physiology 1987, 3:203-210.
80. 2 - do photosynthetic and productivity data from FACE experiments support early predictions?. New Phytologist 2004, 162:253-280.
81. O'Neill E.G. Responses of soil biota to elevated atmospheric carbon dioxide. Plant and Soil 1994, 165:55-65.
82. 2 atmosphere. Canadian Journal of Forest Research 1987, 17:878-883.
83. 2-enrichment and nutrient availability alter ectomycorrhizal fungal communities. Ecology 2006, 87:2278-2287.
84. 2 and nitrogen fertilization. New Phytologist 2007, 176:164-174.
85. 3 on mycorrhizal infection, gas exchange and N metabolism in saplings of Scots pine. Plant and Soil 1995, 176:107-116.
86. 2 increases root exudation from loblolly pine (Pinus taeda) seedlings as an N-mediated response. Tree Physiology 2009, 29:1513-1523.
87. Phillips R.P., Erlitz Y., Bier R., Bernhardt E.S. New approach for capturing soluble root exudates in forest soils. Functional Ecology 2008, 22:990-999.
88. 2 fumigation. Ecology Letters 2011, 14:187-194.
89. Pregitzer K., Loya W., Kubiske M., Zak D. Soil respiration in northern forests exposed to elevated atmospheric carbon dioxide and ozone. Oecologia 2006, 148:503-516.
90. 2-enrichment. Global Change Biology 2008, 14:1-13.
91. 2 exposure. Annals of Botany 1997, 80:809-816.
92. 2. Global Change Biology 2006, 12:1690-1706.
93. Rouhier H., Read D.J. Plant and fungal responses to elevated atmospheric carbon dioxide in mycorrhizal seedlings of Pinus sylvestris. Environmental and Experimental Botany 1998, 40:237-246.
94. 2 in mycorrhizal seedlings of Betula pendula. Environmental and Experimental Botany 1999, 42:231-241.
95. 2 on ectomycorrhiza of longleaf pine. New Phytologist 1997, 137:681-689.
96. 2 and temperature. Oecologia 2000, 124:299-308.
97. Schimel D.S. Terrestrial ecosystems and the carbon cycle. Global Change Biology 1995, 1:77-91.
98. Schimel J.P., Weintraub M.N. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biology & Biochemistry 2003, 35:549-563.
99. 2 on sulphur nutrition of young pedunculate oak (Quercus robur L.) trees. Plant, Cell & Environment 1996, 19:418-426.
100. Smith S.E., Read D.J. Mycorrhizal Symbiosis 1997, Academic Press, London, UK.
101. 2: a simple carbon partitioning model. Plant and Soil 1998, 205:171-180.
102. Stark S., Kytöviita M.-M. Evidence of antagonistic interactions between rhizosphere microorganisms and mycorrhizal fungi associates with birch (Betula pubescens). Acto Oecologica 2005, 28:149-155.
103. Sun Y.-P., Unestam T., Lucas S.D., Johanson K.J., Kenne L., Finlay R.D. Exudation-reabsorption in mycorrhizal fungi, the dynamic interface for interaction with soil and microorganisms. Mycorrhiza 1999, 9:137-144.
104. Taylor A.F.S., Martin F., Read D.J. Fungal diversity in ectomycorrhizal communities of Norway spruce (Picea abies [L.] Karst.) and beech (Fagus sylvatica L.) along north-south transects in Europe. Carbon and Nitrogen Cycling in European Forest Ecosystems 2000, 343-365. Springer Verlag, Berlin, Germany. E.-D. Schulze (Ed.).
105. 2 and nitrogen on the synchrony of shoot and root growth in ponderosa pine. Tree Physiology 1996, 16:905-914.
106. 2 and conifer roots: effects on growth life span and turnover. New Phytologist 2000, 147:87-104.
107. 2 and N fertilization on fine root dynamics and fungal growth in seedling Pinus ponderosa. Environmental Experimental Botany 1997, 37:73-83.
108. 3 on soil respiration under ponderosa pine. Soil Biology and Biochemistry 2006, 38:1764-1778.
109. 2 in field studies. New Phytologist 2004, 164:347-355.
110. Turnau K., Berger A., Loewe A., Einig W., Hampp R., Chalot M., Dizengremel P., Kottke I. Carbon dioxide concentration and nitrogen input affect the C and N storage pools in Amanita muscaria-Picea abies mycorrhizae. Tree Physiology 2001, 21:93-99.
111. van Hees P.A.W., Jones D.L., Finlay R.D., Godbold D.L., Lundström U.S. The C we do not see - the impact of low molecular weight compounds on C dynamics and respiration in forest soils: a review. Soil Biology and Biochemistry 2005, 37:1-13.
112. van Hees P.A.W., Jones D.L., Jentschke G., Godbold D.L. Organic acid concentrations in soil solution: effects of young coniferous trees and ectomycorrhizal fungi. Soil Biology and Biochemistry 2005, 37:771-776.
113. van Hees P.A.W., Rosling A., Esseén S., Godbold D.L., Jones D.L., Finlay R.D. Oxalate and ferricrocin exudation by the extramatrical mycelium of an ectomycorrhizal fungus in symbiosis with Pinus sylvestris. New Phytologist 2006, 169:367-378.
114. 2 and N fertilization on soil respiration from ponderosa pine [Pinus ponderosa] in open-top chambers. Canadian Journal of Forest Research 1995, 25:1243-1251.
115. 2 and soil N fertility effects on growth, mycorrhizal colonization, and xylem water potential of juvenile ponderosa pine in a field soil. Plant and Soil 1997, 195:25-36.
116. 2 and soil P effects on growth and ectomycorrhizal colonization of juvenile ponderosa pine. Forest Ecology and Management 1995, 78:207-215.
117. 2 and soil N and P. Forest Ecology and Management 1998, 109:9-20.
118. Wallander H., Nilsson L.O., Hagerberg D., Bååth E. Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phytologist 2001, 151:753-760.
119. Wallander H., Nilsson L.O., Hagerberg D., Rosengren U. Direct estimates of C:N ratios of ectomycorrhizal mycelia collected from Norway spruce forest soils. Soil Biology and Biochemistry 2003, 35:997-999.
120. Weigt R.B., Raidl R., Verma R., Rodenkirchen H., Göttlein A., Agerer R. Effects of twice-ambient carbon dioxide and nitrogen amendment on biomass, nutrient contents and carbon costs of Norway spruce seedlings as influenced by mycorrhization with Piloderma croceum and Tomentellopsis submollis. Mycorrhiza 2011, 21:375-391.
121. 2 enrichment and nitrogen fertilization. Plant and Soil 2001, 234:99-108.
122. Wiemken V., Laczko E., Ineichen K., Boller T. Effects of elevated carbon dioxide and nitrogen fertilization on mycorrhizal fine roots and the soil microbial community in beech-spruce ecosystems on siliceous and calcareous soil. Microbial Ecology 2001, 42:126-135.
123. Yarwood S.A., Myrold D.D., Högberg M.N. Termination of belowground C allocation by trees alters soil fungal and bacterial communities in a boreal forest. FEMS Microbiology Ecology 2009, 70:151-162.
124. 2 and the composition and function of soil microbial communities. Ecological Applications 2000, 10:47-59.
125. 2 and feedback between carbon and nitrogen cycles. Plant and Soil 1993, 151:105-117.
126. 2, fine roots and the response of soil microorganisms: a review and hypothesis. New Phytologist 2000, 147:201-222.
127. 2. Pedosphere 2010, 20:427-435.