No retraction, correction or concern found when last checked on Nov 2, 2026.
Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil
Christina Kaiser, Marianne Koranda, Barbara Kitzler and 7 more
New Phytologist · 2010
doi:10.1111/j.1469-8137.2010.03321.x
Abstract
*Plant seasonal cycles alter carbon (C) and nitrogen (N) availability for soil microbes, which may affect microbial community composition and thus feed back on microbial decomposition of soil organic material and plant N availability. The temporal dynamics of these plant-soil interactions are, however, unclear. *Here, we experimentally manipulated the C and N availability in a beech forest through N fertilization or tree girdling and conducted a detailed analysis of the seasonal pattern of microbial community composition and decomposition processes over 2 yr. *We found a strong relationship between microbial community composition and enzyme activities over the seasonal course. Phenoloxidase and peroxidase activities were highest during late summer, whereas cellulase and protease peaked in late autumn. Girdling, and thus loss of mycorrhiza, resulted in an increase in soil organic matter-degrading enzymes and a decrease in cellulase and protease activity. *Temporal changes in enzyme activities suggest a switch of the main substrate for decomposition between summer (soil organic matter) and autumn (plant litter). Our results indicate that ectomycorrhizal fungi are possibly involved in autumn cellulase and protease activity. Our study shows that, through belowground C allocation, trees significantly alter soil microbial communities, which may affect seasonal patterns of decomposition processes.
Shown for reading. Its publisher allows quoting it, not republishing it.
References 68
- 1.
Allison SD, Czimczik CI, Treseder KK. Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest. Global Change Biology. 2008;14:1156-1168.
Not in our library
- 2.
Anderson MJ, Willis TJ. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology. 2003;84:511-525.
Not in our library
- 3.
Baldrian P. Ectomycorrhizal fungi and their enzymes in soils: is there enough evidence for their role as facultative soil saprotrophs? Oecologia. 2009;161:657-660.
Not in our library10.1007/s00442-009-1433-7
- 4.
Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK. A temporal approach to linking aboveground and belowground ecology. Trends in Ecology & Evolution. 2005;20:634-641.
Not in our library10.1016/j.tree.2005.08.005
- 5.
Boschker HTS, Bertilsson SA, Dekkers EMJ, Cappenberg TE. An inhibitor-based method to measure initial decomposition of naturally-occurring polysaccharides in sediments. Applied and Environmental Microbiology. 1995;61:2186-2192.
Not in our library10.1128/aem.61.6.2186-2192.1995
- 6.
Brant JB, Myrold DD, Sulzman EW. Root controls on soil microbial community structure in forest soils. Oecologia. 2006;148:650-659.
Not in our library10.1007/s00442-006-0402-7
- 7.
Buee M, Courty PE, Mignot D, Garbaye J. Soil niche effect on species diversity and catabolic activities in an ectomycorrhizal fungal community. Soil Biology & Biochemistry. 2007;39:1947-1955.
Not in our library
- 8.
Butler JL, Williams MA, Bottomley PJ, Myrold DD. Microbial community dynamics associated with rhizosphere carbon flow. Applied and Environmental Microbiology. 2003;69:6793-6800.
Not in our library10.1128/aem.69.11.6793-6800.2003
- 9.
Carney KM, Hungate BA, Drake BG, Megonigal JP. Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proceedings of the National Academy of Sciences, USA. 2007;104:4990-4995.
Not in our library10.1073/pnas.0610045104
- 10.
Courty PE, Breda N, Garbaye J. Relation between oak tree phenology and the secretion of organic matter degrading enzymes by Lactarius quietus ectomycorrhizas before and during bud break. Soil Biology & Biochemistry. 2007;39:1655-1663.
Not in our library
- 11.
Cullings K, Courty PE. Saprotrophic capabilities as functional traits to study functional diversity and resilience of ectomycorrhizal community. Oecologia. 2009;161:661-664.
Not in our library10.1007/s00442-009-1434-6
- 12.
Cullings K, Ishkhanova G, Henson J. Defoliation effects on enzyme activities of the ectomycorrhizal fungus Suillus granulatus in a Pinus contorta (lodgepole pine) stand in Yellowstone National Park. Oecologia. 2008;158:77-83.
Not in our library10.1007/s00442-008-1119-6
- 13.
Dannenmann M, Simon J, Gasche R, Holst J, Naumann PS, Koegel-Knabner I, Knicker H, Mayer H, Schloter M, Pena R, et al. Tree girdling provides insight on the role of labile carbon in nitrogen partitioning between soil microorganisms and adult European beech. Soil Biology & Biochemistry. 2009;41:1622-1631.
Not in our library
- 14.
De Nobili M, Contin M, Mondini C, Brookes PC. Soil microbial biomass is triggered into activity by trace amounts of substrate. Soil Biology & Biochemistry. 2001;33:1163-1170.
Not in our library
- 15.
Dijkstra FA, Cheng WX. Interactions between soil and tree roots accelerate long-term soil carbon decomposition. Ecology Letters. 2007;10:1046-1053.
Not in our library10.1111/j.1461-0248.2007.01095.x
- 16.
Ekberg A, Buchmann N, Gleixner G. Rhizospheric influence on soil respiration and decomposition in a temperate Norway spruce stand. Soil Biology & Biochemistry. 2007;39:2103-2110.
Not in our library
- 17.
Fontaine S, Mariotti A, Abbadie L. The priming effect of organic matter: a question of microbial competition? Soil Biology & Biochemistry. 2003;35:837-843.
Not in our library
- 18.
Frostegård A, Tunlid A, Bååth E. Microbial biomass measured as total lipid phosphate in soils of different organic content. Journal of Microbiological Methods. 1991;14:151-163.
Not in our library
- 19.
Gonzalez I, Dejean S, Martin PGP, Baccini A. CCA: an R package to extend canonical correlation analysis. Journal of Statistical Software. 2008;23:1-14.
Not in our library
- 20.
Guo DL, Li H, Mitchell RJ, Han WX, Hendricks JJ, Fahey TJ, Hendrick RL. Fine root heterogeneity by branch order: exploring the discrepancy in root turnover estimates between minirhizotron and carbon isotopic methods. New Phytologist. 2008;177:443-456.
Not in our library10.1111/j.1469-8137.2007.02242.x
- 21.
Harrison KA, Bol R, Bardgett RD. Do plant species with different growth strategies vary in their ability to compete with soil microbes for chemical forms of nitrogen? Soil Biology & Biochemistry. 2008;40:228-237.
Not in our library
- 22.
Hatakka A, Hofrichter M, Steinbüchel A. Biodegradation of lignin. Biopolymers Vol. 1: Lignin, humic substances and coal. 2001;130-167.
Not in our library
- 23.
Hill GT, Mitkowski NA, Aldrich-Wolfe L, Emele LR, Jurkonie DD, Ficke A, Maldonado-Ramirez S, Lynch ST, Nelson EB. Methods for assessing the composition and diversity of soil microbial communities. Applied Soil Ecology. 2000;15:25-36.
Not in our library
- 24.
Hobbie EA, Horton TR. Evidence that saprotrophic fungi mobilise carbon and mycorrhizal fungi mobilise nitrogen during litter decomposition. New Phytologist. 2007;173:447-449.
Not in our library10.1111/j.1469-8137.2007.01984.x
- 25.
Högberg MN. Discrepancies between ergosterol and the phospholipid fatty acid 18: 2 omega 6,9 as biomarkers for fungi in boreal forest soils. Soil Biology & Biochemistry. 2006;38:3431-3435.
Not in our library
- 26.
Högberg MN, Högberg P, Myrold DD. Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three? Oecologia. 2007;150:590-601.
Not in our library10.1007/s00442-006-0562-5
- 27.
Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Lofvenius M, Read DJ. Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature. 2001;411:789-792.
Not in our library10.1038/35081058
- 28.
Joergensen RG, Wichern F. Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biology & Biochemistry. 2008;40:2977-2991.
Not in our library
- 29.
Jones DL, Hodge A, Kuzyakov Y. Plant and mycorrhizal regulation of rhizodeposition. New Phytologist. 2004;163:459-480.
Not in our library10.1111/j.1469-8137.2004.01130.x
- 30.
Jordan MO, Habib R, Bonafous M. Uptake and allocation of nitrogen in young peach trees as affected by the amount of photosynthates available in roots. Journal of Plant Nutrition. 1998;21:2441-2454.
Not in our library
- 31.
Kaiser C, Frank A, Wild B, Koranda M, Richter A. Negligible contribution from roots to soil-borne phospholipid fatty acid fungal biomarkers 18:2ω6,9 and 18:1ω9. Soil Biology and Biochemistry. 2010.
Not in our library10.1016/j.soilbio.2010.05.019
- 32.
Keeler BL, Hobbie SE, Kellogg LE. Effects of long-term nitrogen addition on microbial enzyme activity in eight forested and grassland sites: implications for litter and soil organic matter decomposition. Ecosystems. 2009;12:1-15.
Not in our library
- 33.
Kielland K, Olson K, Ruess RW, Boone RD. Contribution of winter processes to soil nitrogen flux in taiga forest ecosystems. Biogeochemistry. 2006;81:349-360.
Not in our library
- 34.
Kitzler B, Zechmeister-Boltenstern S, Holtermann C, Skiba U, Butterbach-Bahl K. Nitrogen oxides emission from two beech forests subjected to different nitrogen loads. Biogeosciences. 2006;3:293-310.
Not in our library
- 35.
Kuzyakov Y. Review: factors affecting rhizosphere priming effects. Journal of Plant Nutrition and Soil Science-Zeitschrift Fur Pflanzenernahrung Und Bodenkunde. 2002;165:382-396.
Not in our library
- 36.
Kuzyakov Y, Blagodatskaya E, Blagodatsky S. Comments on the paper by Kemmitt et al. (2008) ‘Mineralization of native soil organic matter is not regulated by the size, activity or composition of the soil microbial biomass – A new perspective’ [Soil Biology & Biochemistry 40, 61–73]: The biology of the Regulatory Gate. Soil Biology & Biochemistry. 2009;41:435-439.
Not in our library
- 37.
Laczko E, Boller T, Wiemken V. Lipids in roots of Pinus sylvestris seedlings and in mycelia of Pisolithus tinctorius during ectomycorrhiza formation: changes in fatty acid and sterol composition. Plant, Cell & Environment. 2004;27:27-40.
Not in our library
- 38.
Leckie SE. Methods of microbial community profiling and their application to forest soils. Forest Ecology and Management. 2005;220:88-106.
Not in our library
- 39.
Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Hogberg P, Stenlid J, Finlay RD. Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytologist. 2007;173:611-620.
Not in our library10.1111/j.1469-8137.2006.01936.x
- 40.
Lipson DA, Schmidt SK, Monson RK. Links between microbial population dynamics and nitrogen availability in an alpine ecosystem. Ecology. 1999;80:1623-1631.
Not in our library
- 41.
Luis P, Kellner H, Zimdars B, Langer U, Martin F, Buscot F. Patchiness and spatial distribution of laccase genes of ectomycorrhizal, saprotrophic, and unknown basidiomycetes in the upper horizons of a mixed forest cambisol. Microbial Ecology. 2005;50:570-579.
Not in our library10.1007/s00248-005-5047-2
- 42.
Marx MC, Wood M, Jarvis SC. A microplate fluorimetric assay for the study of enzyme diversity in soils. Soil Biology & Biochemistry. 2001;33:1633-1640.
Not in our library
- 43.
Moore S. Amino acid analysis – aqueous dimethyl sulfoxide as solvent for ninhydrin reaction. Journal of Biological Chemistry. 1968;243:6281.
Not in our library
- 44.
Newman EI. A method of estimating total length of root in a sample. Journal of Applied Ecology. 1966;3:139.
Not in our library
- 45.
Paterson E. Comments on the regulatory gate hypothesis and implications for C-cycling in soil. Soil Biology & Biochemistry. 2009;41:1352-1354.
Not in our library
- 46.
Phillips RP, Erlitz Y, Bier R, Bernhardt ES. New approach for capturing soluble root exudates in forest soils. Functional Ecology. 2008;22:990-999.
Not in our library
- 47.
Pritchard SG, Strand AE. Can you believe what you see? Reconciling minirhizotron and isotopically derived estimates of fine root longevity. New Phytologist. 2008;177:287-291.
Not in our library10.1111/j.1469-8137.2007.02335.x
- 48.
Prosser JI, Bohannan BJM, Curtis TP, Ellis RJ, Firestone MK, Freckleton RP, Green JL, Green LE, Killham K, Lennon JJ, et al. Essay – the role of ecological theory in microbial ecology. Nature Reviews Microbiology. 2007;5:384-392.
Not in our library10.1038/nrmicro1643
- 49.
Read DJ, Perez-Moreno J. Mycorrhizas and nutrient cycling in ecosystems – a journey towards relevance? New Phytologist. 2003;157:475-492.
Not in our library10.1046/j.1469-8137.2003.00704.x
- 50.
Ruess RW, Hendrick RL, Burton AJ, Pregitzer KS, Sveinbjornsson B, Allen ME, Maurer GE. Coupling fine root dynamics with ecosystem carbon cycling in black spruce forests of interior Alaska. Ecological Monographs. 2003;73:643-662.
Not in our library
- 51.
Saiya-Cork KR, Sinsabaugh RL, Zak DR. The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biology & Biochemistry. 2002;34:1309-1315.
Not in our library
- 52.
Schimel J, Balser TC, Wallenstein M. Microbial stress-response physiology and its implications for ecosystem function. Ecology. 2007;88:1386-1394.
Not in our library10.1890/06-0219
- 53.
Schimel JP, Weintraub MN. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biology & Biochemistry. 2003;35:549-563.
Not in our library
- 54.
Schmidt SK, Costello EK, Nemergut DR, Cleveland CC, Reed SC, Weintraub MN, Meyer AF, Martin AM. Biogeochemical consequences of rapid microbial turnover and seasonal succession in soil. Ecology. 2007;88:1379-1385.
Not in our library10.1890/06-0164
- 55.
Scott-Denton LE, Rosenstiel TN, Monson RK. Differential controls by climate and substrate over the heterotrophic and rhizospheric components of soil respiration. Global Change Biology. 2006;12:205-216.
Not in our library
- 56.
Sinsabaugh RL, Klug MJ, Collins HP, Yeager PE, Petersen SO, Robertson GP, Coleman DC, Bledsoe CS, Sollins P. Characterizing soil microbial communities. Standard soil methods for long-term ecological research. 1999;318-348.
Not in our library
- 57.
Stemmer M, Gerzabek MH, Kandeler E. Organic matter and enzyme activity in particle-size fractions of soils obtained after low-energy sonication. Soil Biology & Biochemistry. 1998;30:9-17.
Not in our library
- 58.
Strickland MS, Lauber C, Fierer N, Bradford MA. Testing the functional significance of microbial community composition. Ecology. 2009;90:441-451.
Not in our library10.1890/08-0296.1
- 59.
Subke JA, Hahn V, Battipaglia G, Linder S, Buchmann N, Cotrufo MF. Feedback interactions between needle litter decomposition and rhizosphere activity. Oecologia. 2004;139:551-559.
Not in our library10.1007/s00442-004-1540-4
- 60.
Talbot JM, Allison SD, Treseder KK. Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Functional Ecology. 2008;22:955-963.
Not in our library
- 61.
Waldrop MP, Zak DR. Response of oxidative enzyme activities to nitrogen deposition affects soil concentrations of dissolved organic carbon. Ecosystems. 2006;9:921-933.
Not in our library
- 62.
Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH. Ecological linkages between aboveground and belowground biota. Science. 2004;304:1629-1633.
Not in our library10.1126/science.1094875
- 63.
Watanabe K, Hayano K. Seasonal-variation of soil protease activities and their relation to proteolytic bacteria and Bacillus spp. in paddy field soil. Soil Biology & Biochemistry. 1995;27:197-203.
Not in our library
- 64.
Weintraub MN, Schimel JP. Seasonal protein dynamics in Alaskan arctic tundra soils. Soil Biology & Biochemistry. 2005;37:1469-1475.
Not in our library
- 65.
Weintraub MN, Scott-Denton LE, Schmidt SK, Monson RK. The effects of tree rhizodeposition on soil exoenzyme activity, dissolved organic carbon, and nutrient availability in a subalpine forest ecosystem. Oecologia. 2007;154:327-338.
Not in our library10.1007/s00442-007-0804-1
- 66.
Yarwood SA, Myrold DD, Hogberg MN. Termination of belowground C allocation by trees alters soil fungal and bacterial communities in a boreal forest. FEMS Microbiology Ecology. 2009;70:151-162.
Not in our library10.1111/j.1574-6941.2009.00733.x
- 67.
Zeller B, Liu JX, Buchmann N, Richter A. Tree girdling increases soil N mineralisation in two spruce stands. Soil Biology & Biochemistry. 2008;40:1155-1166.
Not in our library
- 68.
Zelles L. Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere. 1997;35:275-294.
Not in our library10.1016/s0045-6535(97)00155-0
Cited by papers we hold 3
- A starting guide to root ecology: strengthening ecological concepts and standardising root classification, sampling, processing and trait measurements · 2021Corrected
- Ecological memory of recurrent drought modifies soil processes via changes in soil microbial community · 2021No notice
- Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow · 2013No notice
Reads
Read by people on this page
None yet.
Checked or read by AI through naulon
None yet.
A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.
Are you an author?
Is this your paper?
Claim it to add your note and be paid when agents cite it. Free.