Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil

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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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

Cited by papers we hold 3

• A starting guide to root ecology: strengthening ecological concepts and standardising root classification, sampling, processing and trait measurements · 2021
  Corrected
• Ecological memory of recurrent drought modifies soil processes via changes in soil microbial community · 2021
  No notice
• Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow · 2013
  No notice

Reads

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.