Water, Air, & Soil Pollution

, Volume 216, Issue 1–4, pp 229–237 | Cite as

Mixed Inorganic and Organic Nitrogen Addition Enhanced Extracellular Enzymatic Activities in a Subtropical Forest Soil in East China

  • Peng Guo
  • Congyan Wang
  • Xiaoguang Feng
  • Minfei Su
  • Wenqing Zhu
  • Xingjun TianEmail author


To date, numerous studies have employed single type nitrogen (N) addition methods in reporting influences of N deposition on soil extracellular enzymatic activities (EEA) during litter decomposition in forest ecosystems. As natural atmospheric N deposition is a set of complex compounds including inorganic N and organic N, it is essential for investigating responses of soil EEA to various mixed N fertilization. In a subtropical forest stand in Zijin Mountain, East China, various N fertilizers with different inorganic N and organic N ratios were added to soils monthly from 2008 to 2009. Samples were harvested from N fertilized and control plots every 4 months. Subsequently, six EEA were assayed. A laboratory experiment was also conducted simultaneously. Both field and laboratory experiments showed that various mixed N fertilizations revealed different influences on soil EEA. Acceleration of most soil EEA by mixed N fertilization was greater than that of single N fertilization. The majority of soil extracellular enzymes exhibited the highest activities under mixed N fertilization, with the ratio of inorganic N to organic N at 3:7. These results suggested that N type and ratio of inorganic N and organic N were important factors controlling soil EEA, and the 3:7 ratio of inorganic N and organic N may be the optimum for soil EEA.


Extracellular enzyme activity Forest soil Inorganic nitrogen Nitrogen deposition Organic nitrogen 



This study was supported by Project of National Science Foundation (30870419), the National Basic Research Program (2008CB418004) of China.


  1. Aber, J. D., Goodale, C. L., Ollinger, S. V., Smith, M. L., Magill, A. H., Martin, M. E., et al. (2003). Is nitrogen deposition altering the nitrogen status of northeastern forests? Bioscience, 53, 375–389.CrossRefGoogle Scholar
  2. Ajwa, H. A., Dell, C. J., & Rice, C. W. (1999). Changes in enzyme activities and microbial biomass of tallgrass prairie soil as related to burning and nitrogen fertilization. Soil Biology and Biochemistry, 31, 769–777.CrossRefGoogle Scholar
  3. Alvarez, S., & Guerrero, M. C. (2000). Enzymatic activities associated with decomposition of particulate organic matter in two shallow ponds. Soil Biology and Biochemistry, 32, 1941–1951.CrossRefGoogle Scholar
  4. Bailey, V. L., Peacock, A. D., Smith, J. L., & Bolton, H. (2002). Relationships between soil microbial biomass determined by chloroform fumigation-extraction, substrate-induced respiration, and phospholipid fatty acid analysis. Soil Biology and Biochemistry, 34, 1385–1389.CrossRefGoogle Scholar
  5. Bragazza, L., Freeman, C., Jones, T., Rydin, H., Limpens, J., Fenner, N., et al. (2006). Atmospheric nitrogen deposition promotes carbon loss from peat bogs. Proceedings of the National Academy of Sciences of the United States of America, 103, 19386–19389.CrossRefGoogle Scholar
  6. Breeuwer, A., Heijmans, M., Robroek, B. J. M., Limpens, J., & Berendse, F. (2008). The effect of increased temperature and nitrogen deposition on decomposition in bogs. Oikos, 117, 1258–1268.CrossRefGoogle Scholar
  7. Bytnerowicz, A., & Fenn, M. E. (1996). Nitrogen deposition in California forests: A review. Environmental Pollution, 92, 127–146.CrossRefGoogle Scholar
  8. Caldwell, B. A. (2005). Enzyme activities as a component of soil biodiversity: A review. Pedobiologia, 49, 637–644.CrossRefGoogle Scholar
  9. Carreiro, M. M., Sinsabaugh, R. L., Repert, D. A., & Parkhurst, D. F. (2000). Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology, 81, 2359–2365.CrossRefGoogle Scholar
  10. Chen, X. Y., & Mulder, J. (2007). Atmospheric deposition of nitrogen at five subtropical forested sites in South China. The Science of the Total Environment, 378, 317–330.CrossRefGoogle Scholar
  11. Cornell, S. E., Jickells, T. D., Cape, J. N., Rowland, A. P., & Duce, R. A. (2003). Organic nitrogen deposition on land and coastal environments: A review of methods and data. Atmospheric Environment, 37, 2173–2191.CrossRefGoogle Scholar
  12. Cornell, S., Mace, K., Coeppicus, S., Duce, R., Huebert, B., Jickells, T., et al. (2001). Organic nitrogen in Hawaiian rain and aerosol. Journal of Geophysical Research, [Atmospheres], 106, 7973–7983.CrossRefGoogle Scholar
  13. Daniel, R. M., & Curran, M. P. (1981). A method for the determination of nitrate reductase. Journal of Biochemical and Biophysical Methods, 4, 131–132.CrossRefGoogle Scholar
  14. Deng, S. P., & Tabatabai, M. A. (1994). Cellulase activity of soils. Soil Biology and Biochemistry, 26, 1347–1354.CrossRefGoogle Scholar
  15. Deng, S. P., & Tabatabai, M. A. (1997). Effect of tillage and residue management on enzyme activities in soils.3. Phosphatases and arylsulfatase. Biology and Fertility of Soils, 24, 141–146.CrossRefGoogle Scholar
  16. Dick, W. A., Cheng, L., & Wang, P. (2000). Soil acid and alkaline phosphatase activity as pH adjustmentindicators. Soil Biology and Biochemistry, 32, 1915–1919.CrossRefGoogle Scholar
  17. Dilly, O., & Nannipieri, P. (1998). Intracellular and extracellular enzyme activity in soil with reference to elemental cycling. Zeitschrift Fur Pflanzenernahrung Und Bodenkunde, 161, 243–248.Google Scholar
  18. Enowashu, E., Poll, C., Lamersdorf, N., & Kandeler, E. (2009). Microbial biomass and enzyme activities under reduced nitrogen deposition in a spruce forest soil. Applied Soil Ecology, 43, 11–21.CrossRefGoogle Scholar
  19. Ghose, T. K. (1987). Measurement of cellulase activities. Pure and Applied Chemistry, 59, 257–268.CrossRefGoogle Scholar
  20. Grandy, A., Sinsabaugh, R., Neff, J., Stursova, M., & Zak, D. (2008). Nitrogen deposition effects on soil organic matter chemistry are linked to variation in enzymes, ecosystems and size fractions. Biogeochemistry, 91, 37–49.CrossRefGoogle Scholar
  21. Jones, D. L., Shannon, D., Murphy, D. V., & Farrar, J. (2004). Role of dissolved organic nitrogen (DON) in soil N cycling in grassland soils. Soil Biology and Biochemistry, 36, 749–756.CrossRefGoogle Scholar
  22. Juma, N. G., & Tabatabai, M. A. (1977). Effects of trace-elements on phosphatase-activity in soils. Soil Science Society of America Journal, 41, 343–346.CrossRefGoogle Scholar
  23. Kandeler, E., Tscherko, D., & Spiegel, H. (1999). Long-term monitoring of microbial biomass, N mineralisation and enzyme activities of a Chernozem under different tillage management. Biology and Fertility of Soils, 28, 343–351.CrossRefGoogle Scholar
  24. Manning, P., Saunders, M., Bardgett, R. D., Bonkowski, M., Bradford, M. A., Ellis, R. J., et al. (2008). Direct and indirect effects of nitrogen deposition on litter decomposition. Soil Biology and Biochemistry, 40, 688–698.CrossRefGoogle Scholar
  25. Matson, P. A., McDowell, W. H., Townsend, A. R., & Vitousek, P. M. (1999). The globalization of N deposition: Ecosystem consequences in tropical environments. Biogeochemistry, 46, 67–83.Google Scholar
  26. Michel, K., & Matzner, E. (2003). Response of enzyme activities to nitrogen addition in forest floors of different C-to-N ratios. Biology and Fertility of Soils, 38, 102–109.CrossRefGoogle Scholar
  27. Nannipieri, P., Ceccanti, B., Cervelli, S., & Matarese, E. (1980). Extraction of Phosphatase, Urease, Proteases, Organic-carbon, and Nitrogen from soil. Soil Science Society of America Journal, 44, 1011–1016.CrossRefGoogle Scholar
  28. Neff, J. C., Holland, E. A., Dentener, F. J., McDowell, W. H., & Russell, K. M. (2002). The origin, composition and rates of organic nitrogen deposition, A missing piece of the nitrogen cycle? Biogeochemistry, 57, 99–136.CrossRefGoogle Scholar
  29. Nohrstedt, H. O., Arnebrant, K., Baath, E., & Soderstrom, B. (1989). Changes in carbon content, respiration rate, ATP content, and microbial biomass in nitrogen fertilized pine forest soils in Sweden. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere, 19, 323–328.CrossRefGoogle Scholar
  30. Ohshima, T., Tamura, T., & Sato, M. (2007). Influence of pulsed electric field on various enzyme activities. Journal of Electrostatics, 65, 156–161.CrossRefGoogle Scholar
  31. Saiya-Cork, K. R., Sinsabaugh, R. L., & Zak, D. R. (2002). The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biology and Biochemistry, 34, 1309–1315.CrossRefGoogle Scholar
  32. Sinsabaugh, R. L., Carreiro, M. M., & Repert, D. A. (2002). Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry, 60, 1–24.CrossRefGoogle Scholar
  33. Sinsabaugh, R. L., Gallo, M. E., Lauber, C., Waldrop, M. P., & Zak, D. R. (2005). Extracellular enzyme activities and soil organic matter dynamics for northern hardwood forests receiving simulated nitrogen deposition. Biogeochemistry, 75, 201–215.CrossRefGoogle Scholar
  34. Speir, T. W., & Cowling, J. C. (1991). Phosphatase-activities of pasture plants and soils - relationship with plant productivity and soil-p fertility indexes. Biology and Fertility of Soils, 12, 189–194.CrossRefGoogle Scholar
  35. Thirukkumaran, C. M., & Parkinson, D. (2000). Microbial respiration, biomass, metabolic quotient and litter decomposition in a lodgepole pine forest floor amended with nitrogen and phosphorous fertilizers. Soil Biology and Biochemistry, 32, 59–66.CrossRefGoogle Scholar
  36. Treseder, K. K. (2008). Nitrogen additions and microbial biomass: A meta-analysis of ecosystem studies. Ecology Letters, 11, 1111–1120.CrossRefGoogle Scholar
  37. Wallenstein, M. D., McNulty, S., Fernandez, I. J., Boggs, J., & Schlesinger, W. H. (2006). Nitrogen fertilization decreases forest soil fungal and bacterial biomass in three long-term experiments. Forest Ecology and Management, 222, 459–468.CrossRefGoogle Scholar
  38. Wang, T. J., Jiang, F., Li, S., & Liu, Q. (2007). Trends in air pollution during 1996-2003 and cross-border transport in city clusters over the Yangtze River Delta region of China. Terrestrial Atmospheric and Oceanic Sciences, 18, 995–1009.CrossRefGoogle Scholar
  39. Wang, Q. K., Wang, S. L., & Liu, Y. (2008). Responses to N and P fertilization in a young Eucalyptus dunnii plantation: Microbial properties, enzyme activities and dissolved organic matter. Applied Soil Ecology, 40, 484–490.CrossRefGoogle Scholar
  40. Zhang, Q., Anastasio, C., & Jimemez-Cruz, M. (2002). Water-soluble organic nitrogen in atmospheric fine particles (PM2.5) from northern California. Journal of Geophysical Research Atmospheres, 107, AAC3.1–AAC3.10.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Peng Guo
    • 1
  • Congyan Wang
    • 1
  • Xiaoguang Feng
    • 1
  • Minfei Su
    • 1
  • Wenqing Zhu
    • 1
  • Xingjun Tian
    • 1
    Email author
  1. 1.School of Life ScienceNanjing UniversityNanjingChina

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