Document Type : Research Paper
Authors
Abstract
Increasing nutrient inputs into terrestrial ecosystems affect not only plant communities but also the associated soil microbial ones. Studies carried out in predominantly unmanaged ecosystems have found that increasing nitrogen (N) inputs generally decrease soil microbial biomass while less is known about their long-term impacts on managed systems such as agroecosystems. The objective of this study was to analyze the responses of soil microorganisms to mineral fertilizers using data from long-term fertilization trials in cropping systems. A meta-analysis based on 107 datasets from 64 long-term trials from around the world revealed that mineral fertilizer application led to a 15.1% increase in the microbial biomass (Cmic) above the levels observed in unfertilized control treatments. Mineral fertilization also increased soil organic carbon (Corg) content, suggesting that Corg is a major contributor to the overall increase in Cmic under mineral fertilization. The magnitude of the effect of fertilization on Cmic was found to be pH-dependent. While fertilization tended to reduce Cmic in soils with a pH below 5 in the fertilized treatment, it had a significantly positive effect at higher soil pH values. Duration of the trial also affected the response of Cmic to fertilization, with increases in Cmic most pronounced in studies with a duration of at least 20 years. The input of N per se does not seem to negatively affect Cmic in cropping systems. Application of urea and ammonia fertilizers can, however, temporarily increase pH, osmotic potential, and ammonia concentrations to levels inhibitory to microbial communities. Even though impacts of fertilizers are spatially limited, they may strongly affect soil microbial biomass and community composition in the short term. Long-term repeated mineral N applications may alter microbial community composition even with small changes in pH. The way specific microbial groups respond to repeated applications of mineral fertilizers, however, varies considerably and seems to depend on environmental and crop management related factors.
Keywords
- Aciego Pietri, J.C., Brookes, P.C., 2008. Relationships between soil pH and microbial properties in a UK arable soil. Soil Biology and Biochemistry 40, 1856-1861.
- Acosta-Martínez, V., Zobeck, T.M., Gill, T.E., Kennedy, A.C., 2003. Enzyme activities and microbial community structure in semiarid agricultural soils. Biology and Fertility of Soils 38, 216-227.
- Ai, C., Liang, G., Sun, J., Wang, X., Zhou, W., 2012. Responses of extracellular enzyme activities and microbial community in both the rhizosphere and bulk soil to long-term fertilization practices in a fluvo-aquic soil. Geoderma 173-174, 330- 338.
- Ai, C., Liang, G., Sun, J., Wang, X., He, P., Zhou, W., 2013. Different roles of rhizosphere effect and long-term fertilization in the activity and community structure of ammonia oxidizers in a calcareous fluvo-aquic soil. Soil Biology and Biochemistry 57, 30-42.
- Allison, C., Macfarlane, G.T., 1992. Physiological and nutritional determinants of protease secretion by Clostridium sporogenes: characterization of six extracellular proteases. Applied Microbiology and Biotechnology 37, 152-156.
- Allison, S.D., Martiny, J.B.H., 2008. Resistance, resilience, and redundancy in microbial communities. Proceedings of the National Academy of Sciences of the USA 105, 11512-11519.
- Anderson, T.H., 2003. Microbial eco-physiological indicators to asses soil quality. Agriculture, Ecosystems and Environment 98, 285-293.
- Anderson, T.H., Domsch, K.H., 1989. Ratios of microbial biomass carbon to total organic carbon in arable soils. Soil Biology and Biochemistry 21, 471-479.
- Bååth, E., Anderson, T.H., 2003. Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biology and Biochemistry 35, 955-963.
- Barak, P., Jobe, B.O., Krueger, A.R., Peterson, L.A., Laird, D.A., 1997. Effects of long term soil acidification due to nitrogen fertilizer inputs in Wisconsin. Plant and Soil 197, 61-69.
- Biederbeck, V.O., Campbell, C.A., Ukrainetz, H., Curtin, D., Bouman, O.T., 1996. Soil microbial and biochemical properties after ten years of fertilization with urea and anhydrous ammonia. Canadian Journal of Soil Science 76, 7-14.
- Blagodatskaya, E.V., Anderson, T.H., 1998. Interactive effects of pH and substrate quality on the fungal-to-bacterial ratio and qCO2 of microbial communities in forest soils. Soil Biology and Biochemistry 30, 1269-1274.
- Böhme, L., Langer, U., Böhme, F., 2005. Microbial biomass, enzyme activities and microbial community structure in two European long-term field experiments. Agriculture, Ecosystems and Environment 109, 141-152.
- Booth, M.S., Stark, J.M., Rastetter, E., 2005. Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecological Monographs 75, 139-157.
- Börjesson, G., Menichetti, L., Kirchmann, H., Kätterer, T., 2012. Soil microbial community structure affected by 53 years of nitrogen fertilisation and different organic amendments. Biology and Fertility of Soils 48, 245-257.
- Bossio, D.A., Scow, K.M., Gunapala, N., Graham, K.J., 1998. Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microbial Ecology 36, 1-12.
- 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.
- Chu, H., Fujii, T., Morimoto, S., Lin, X., Yagi, K., Hu, J., Zhang, J., 2007. Community structure of ammonia-oxidizing bacteria under long-term application of mineral fertilizer and organic manure in a sandy loam soil. Applied and Environmental Microbiology 73, 485-491.
- Clark, C.M., Cleland, E.E., Collins, S.L., Fargione, J.E., Gough, L., Gross, K.L., Pennings, S.C., Suding, K.N., Grace, J.B., 2007. Environmental and plant community determinants of species loss following nitrogen enrichment. Ecology Letters 10, 596-607.
- Cleland, E.E., Harpole, W.S., 2010. Nitrogen enrichment and plant communities. Annals of the New York Academy of Sciences 1195, 46-61.
- Cleveland, C.C., Liptzin, D., 2007. C: N: P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85, 235-252.
- Cohen, J., Cohen, P., West, S.G., Aiken, L.S., 2003. Applied Multiple Regression/Correlation Analysis for the Behavioral Sciences, third ed. Lawrence Earlbaum Associates, Mahwah, NJ.
- Deng, S.P., Tabatabai, M.A., 1996. Effect of tillage and residue management on enzyme activities in soils II. Glycosidases. Biology and Fertility of Soils 22, 208- 213.
- Deng, S.P., Parham, J.A., Hattey, J.A., Babu, D., 2006. Animal manure and anhydrous ammonia amendment alter microbial carbon use efficiency, microbial biomass, and activities of dehydrogenase and amidohydrolases in semiarid agroecosystems. Applied Soil Ecology 33, 258-268.
- Dick, W.A., 1984. Influence of long-term tillage and crop rotation combinations on soil enzyme activities. Soil Science Society of America Journal 48, 569-574.
- Eno, C.F., Blue, W.G., Good, J.M., 1955. The effect of anhydrous ammonia on nematodes, fungi, bacteria, and nitrification in some Florida soils. Proceedings of the Soil Science Society of America 19, 55-58.
- Enwall, K., Philippot, L., Hallin, S., 2005. Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Applied and Environmental Microbiology 71, 8335-8343.
- Enwall, K., Nyberg, K., Bertilsson, S., Cederlund, H., Stenström, J., Hallin, S., 2007. Long-term impact of fertilization on activity and composition of bacterial communities and metabolic guilds in agricultural soils. Soil Biology and Biochemistry 39, 106-115.
- Elfstrand, S., Hedlund, K., Mårtensson, A., 2007. Soil enzyme activities, microbial community composition and function after 47 years of continuous green manuring. Applied Soil Ecology 35, 610-621.
- Esperschütz, J., Gattinger, A., Mäder, P., Schloter, M., Fließbach, A., 2007. Response of soil microbial biomass and community structures to conventional and organic farming systems under identical crop rotations. FEMS Microbiology Ecology 61, 26-37.
- Fierer, N., Jackson, R.B., 2006. The diversity and biogeography of soil bacterial communities. Proceedings of the National Academy of Sciences of the USA 103, 626-631.
- Fierer, N., Strickland, M.S., Liptzin, D., Bradford, M.A., Cleveland, C.C., 2009. Global patterns in belowground communities. Ecology Letters 12, 1238-1249.
- Fierer, N., Lauber, C.L., Ramirez, K.S., Zaneveld, J., Bradford, M.A., Knight, R., 2012. Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. The ISME Journal 6, 1007-1017.
- Geisseler, D., Horwath, W.R., 2009. Relationship between carbon and nitrogen availability and extracellular enzyme activities in soil. Pedobiologia 53, 87-98.
- Geisseler, D. and Scow, K.M., 2014. Long-term effects of mineral fertilizers on soil microorganisms–A review. Soil Biology and Biochemistry 75, 54-63.
- Glenn, A.R., 1976. Production of extracellular proteins by bacteria. Annual Review of Microbiology 30, 41-62.
- Guo, J.H., Liu, X.J., Zhang, Y., Shen, J.L., Han, W.X., Zhang, W.F., Christie, P., Goulding, K.W.T., Vitousek, P.M., Zhang, F.S., 2010. Significant acidification in major Chinese croplands. Science 327, 1008-1010.
- Gurevitch, J., Hedges, L.V., 2001. Meta-analysis. In: Scheiner, S.M., Gurevitch, J. (Eds.), Design and Analysis of Ecological Experiments. Oxford University Press, Inc., New York, pp. 347-369.
- Hallin, S., Jones, C.M., Schloter, M., Philippot, L., 2009. Relationship between N cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. The ISME Journal 3, 597-605.
- Harris, J.A., Ritz, K., Coucheney, E., Grice, S.M., Lerch, T.Z., Pawlett, M., Herrmann, A.M., 2012. The thermodynamic efficiency of soil microbial communities subject to long-term stress is lower than those under conventional input regimes. Soil Biology and Biochemistry 47, 149-157.
- Hartmann, M., Fliessbach, A., Oberholzer, H., Widmer, F., 2006. Ranking the magnitude of crop and farming system effects on soil microbial biomass and genetic structure of bacterial communities. FEMS Microbiology Ecology 57, 378-388.
- He, J., Shen, J., Zhang, L., Zhu, Y., Zheng, Y., Xu, M., Di, H., 2007. Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environmental Microbiology 9, 2364-2374.
- Hedges, L.V., Gurevitch, J., Curtis, P.S., 1999. The meta-analysis of response ratios in experimental ecology. Ecology 80, 1150-1156.
- Henriksen, T.M., Breland, T.A., 1999. Nitrogen availability effects on carbon mineralization, fungal and bacterial growth, and enzyme activities during decomposition of wheat straw in soil. Soil Biology and Biochemistry 31, 1121-1134.
- Hou, A., Tsuruta, H., McCreary, M.A., Hosen, Y., 2010. Effect of urea placement on the time-depth profiles of NO, N2O and mineral nitrogen concentrations in an Andisol during a Chinese cabbage growing season. Soil Science and Plant Nutrition 56, 861-869.
- Hu, J., Lin, X., Wang, J., Dai, J., Chen, R., Zhang, J., Wong, M.H., 2011. Microbial functional diversity, metabolic quotient, and invertase activity of a sandy loam soil as affected by long-term application of organic amendment and mineral fertilizer. Journal of Soils and Sediments 11, 271-280.
- Joergensen, R.G., Emmerling, C., 2006. Methods for evaluating human impact on soil microorganisms based on their activity, biomass, and diversity in agricultural soils. Journal of Plant Nutrition and Soil Science 169, 295-309.
- Kallenbach, C., Grandy, A.S., 2011. Controls over soil microbial biomass responses to carbon amendments in agricultural systems: a meta-analysis. Agriculture, Ecosystems and Environment 144, 241-252.
- Kirchmann, H., Persson, J., Carlgren, K., 1994. The Ultuna Long-term Soil Organic Matter Experiment, 1956e1991. Reports and dissertations 17. Department of Soil Sciences, Swedish University of Agricultural Sciences, Uppsala.
- Kirchmann, H., Schön, M., Börjesson, G., Hamnér, K., Kätterer, T., 2013. Properties of soils in the Swedish long-term fertility experiments: VII. Changes in topsoil and upper subsoil at Örja and Fors after 50 years of nitrogen fertilization and manure application. Acta Agriculturae Scandinavica, Section B e Soil and Plant Science 63, 25-36.
- Klose, S., Tabatabai, M.A., 1999. Urease activity of microbial biomass in soils. Soil Biology and Biochemistry 31, 205-211.
- Koper, T.E., Stark, J.M., Habteselassie, M.Y., Norton, J.M., 2010. Nitrification exhibits Haldane kinetics in an agricultural soil treated with ammonium sulfate or dairy-waste compost. FEMS Microbiology Ecology 74, 316-322.
- Körschens, M., Albert, E., Armbruster, M., Barkusky, D., Baumecker, M., BehleSchalk, L., Bischoff, R., Cergan, Z., Ellmer, F., Herbst, F., Hoffmann, S., Hofmann, B., Kismanyoky, T., Kubat, J., Kunzova, E., Lopez-Fando, C., Merbach, I., Merbach, W., Pardor, M.T., Rogasik, J., Rühlmann, J., Spiegel, H., Schulz, E., Tajnsek, A., Toth, Z., Wegener, H., Zorn, W., 2013. Effect of mineral and organic fertilization on crop yield, nitrogen uptake, carbon and nitrogen balances, as well as soil organic carbon content and dynamics: results from 20 European long-term field experiments of the twenty-first century. Archives of Agronomy and Soil Science 59, 1017-1040.
- Ku, H.H., 1966. Notes on the use of propagation of error formulas. Journal of Research of the National Bureau of Standards e C. Engineering and Instrumentation 70C, 263-273.
- Ladha, J.K., Reddy, C.K., Padre, A.T., van Kessel, C., 2011. Role of nitrogen fertilization in sustaining organic matter in cultivated soils. Journal of Environmental Quality 40, 1756-1766.
- Langer, U., Klimanek, E., 2006. Soil microbial diversity of four German long-term field experiments. Archives of Agronomy and Soil Science 52, 507-523.
- Lauber, C.L., Hamady, M., Knight, R., Fierer, N., 2009. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Applied Environmental Microbiology 75, 5111-5120.
- LeBauer, D.S., Treseder, K.K., 2008. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89, 371-379.
- Liu, L., Greaver, T.L., 2010. A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecology Letters 13, 819-828.
- Lu, M., Yang, Y., Luo, Y., Fang, C., Zhou, X., Chen, J., Yang, X., Li, B., 2011. Responses of ecosystem nitrogen cycle to nitrogen addition: a meta-analysis. New Phytologist 189, 1040-1050.
- Lupwayi, N.Z., Clayton, G.W., O’Donovan, J.T., Grant, C.A., 2011. Soil microbial response to nitrogen rate and placement and barley seeding rate under no till. Agronomy Journal 103, 1064-1071.
- Lupwayi, N.Z., Lafond, G.P., Ziadi, N., Grant, C.A., 2012. Soil microbial response to nitrogen fertilizer and tillage in barley and corn. Soil and Tillage Research 118, 139-146.
- Malhi, S.S., Harapiak, J.T., Nyborg, M., Gill, K.S., 2000. Effects of long-term applications of various nitrogen sources on chemical soil properties and composition of bromegrass hay. Journal of Plant Nutrition 23, 903-912.
- Marschner, P., Yang, C.H., Lieberei, R., Crowley, D.E., 2001. Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biology and Biochemistry 33, 1437-1445.
- Marstorp, H., Guan, X., Gong, P., 2000. Relationship between dsDNA, chloroform labile C and ergosterol in soils of different organic matter contents and pH. Soil Biology and Biochemistry 32, 879-882.
- Marzluf, G.A., 1997. Genetic regulation of nitrogen metabolism in the fungi. Microbiology and Molecular Biology Reviews 61, 17-32.
- Merbach, I., Körschens, M., 2002. The static fertilization experiment at the start and the end of the 20th century. Archives of Agronomy and Soil Science 48, 413-422.
- Merrick, M.J., Edwards, R.A., 1995. Nitrogen control in bacteria. Microbiology and Molecular Biology Reviews 59, 604-622.
- Müller, T., Walter, B., Wirtz, A., Burkovski, A., 2006. Ammonium toxicity in bacteria. Current Microbiology 52, 400-406.
- Neumann, D., Heuer, A., Hemkemeyer, M., Martens, R., Tebbe, C.C., 2013. Response of microbial communities to long-term fertilization depends on their microhabitat. FEMS Microbiology Ecology 86, 71-84.
- Nicol, G.W., Leininger, S., Schleper, C., Prosser, J.I., 2008. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environmental Microbiology 10, 2966-2978.
- Ogilvie, L.A., Hirsch, P.R., Johnston, A.W.B., 2008. Bacterial diversity of the Broadbalk ‘Classical’ winter wheat experiment in relation to long-term fertilizer inputs. Microbial Ecology 56, 525-537.
- Omar, S.A., Ismail, M., 1999. Microbial populations, ammonification and nitrification in soil treated with urea and inorganic salts. Folia Microbiologica 44, 205-212.
- Peacock, A.D., Mullen, M.D., Ringelberg, D.B., Tyler, D.D., Hedrick, D.B., Gale, P.M., White, D.C., 2001. Soil microbial community responses to dairy manure or ammonium nitrate applications. Soil Biology and Biochemistry 33, 1011-1019.
- Peigné, J., Vian, J.F., Cannavacciuolo, M., Bottollier, B., Chaussod, R., 2009. Soil sampling based on field spatial variability of soil microbial indicators. European Journal of Soil Biology 45, 488-495.
- Pelster, D.E., Larouche, F., Rochette, P., Chantigny, M.H., Allaire, S., Angers, D.A., 2011. Nitrogen fertilization but not soil tillage affects nitrous oxide emissions from a clay loam soil under a maize-soybean rotation. Soil and Tillage Research 115-116, 16e26.
- Pierre, W.H., 1928. Nitrogenous fertilizers and soil acidity: I. Effect of various nitrogenous fertilizers on soil reaction. Journal of the American Society of Agronomy 20, 254-269.
- Prosser, J.I., Nicol, G.W., 2012. Archaeal and bacterial ammonia oxidisers in soil: the quest for niche specialisation and differentiation. Trends in Microbiology 20, 523-531.
- Ramirez, K.S., Lauber, C.L., Knight, R., Bradford, M.A., Fierer, N., 2010. Consistent effects of nitrogen fertilization on soil bacterial communities in contrasting systems. Ecology 91, 3463-3470.
- Roberts, B.A., Fritschi, F.B., Horwath, W.R., Scow, K.M., Rains, W.D., Travis, R.L., 2011. Comparisons of soil microbial communities influenced by soil texture, nitrogen fertility, and rotations. Soil Science 176, 487-494.
- Robertson, G.P., Vitousek, P.M., 2009. Nitrogen in agriculture: balancing the cost of an essential resource. Annual Review of Environment and Resources 34, 97- 125.
- Rosenberg, S.M., 2013. Moment and least-squares based approaches to Meta analytic inference. In: Koricheva, J., Gurevitch, J., Mengersen, K. (Eds.), Handbook of Meta-analysis in Ecology and Evolution. Princeton University Press, Princeton, NJ, pp. 108-124.
- Rosenberg, S.M., Rothstein, H.R., Gurevitch, J., 2013. Effect sizes: conventional choices and calculations. In: Koricheva, J., Gurevitch, J., Mengersen, K. (Eds.), Handbook of Meta-analysis in Ecology and Evolution. Princeton University Press, Princeton, NJ, pp. 61-71.
- Rothamsted Research, 2006. Guide to the Classical and Other Long-term Experiments, Datasets and Sample Archive. Premier Printers Ltd., Bury St Edmunds, Suffolk, UK.
- Rousk, J., Brookes, P.C., Bååth, E., 2009. Contrasting soil pH effects on fungal and bacterial growth suggests functional redundancy in carbon mineralisation. Applied and Environmental Microbiology 75, 1589-1596.
- Sakamoto, K., Oba, Y., 1994. Effect of fungal to bacterial biomass ratio on the relationship between CO2 evolution and total soil microbial biomass. Biology and Fertility of Soils 17, 39-44.
- Schneider, S., Hartmann, M., Enkerli, J., Widmer, F., 2010. Fungal community structure in soils of conventional and organic farming systems. Fungal Ecology 3, 215-224.
- Schroder, J.L., Zhang, H., Girma, K., Raun, W.R., Penn, C.J., Payton, M.E., 2011. Soil acidification from long-term use of nitrogen fertilizers on winter wheat. Soil Science Society of America Journal 75, 957-964.
- Schwab, A.P., Owensby, C.E., Kulyingyong, S., 1990. Changes in soil chemical properties due to 40 years of fertilization. Soil Science 149, 35-43.
- Setua, G.C., Samaddar, K.R., 1980. Evaluation of role of volatile ammonia in fungistasis of soils. Phytopathologische Zeitschrift 98, 310-319.
- Shen, J., Zhang, L., Zhu, Y., Zhang, J., He, J., 2008. Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environmental Microbiology 10, 1601-1611.
- Stange, C.F., Neue, H.U., 2009. Measuring and modelling seasonal variation of gross nitrification rates in response to long-term fertilization. Biogeosciences 6, 2181-2192.
- Stark, C., Condron, L.M., Stewart, A., Di, H.J., O’Callaghan, M., 2007. Influence of organic and mineral amendments on microbial soil properties and processes. Applied Soil Ecology 35, 79-93.
- Treseder, K.K., 2008. Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecology Letters 11, 1111-1120.
- Vitousek, P.M., Aber, J.D., Howarth, R.W., Likens, G.E., Matson, P.A., Schindler, D.W., Schlesinger, W.H., Tilman, D.G., 1997. Human alteration of the global nitrogen cycle: sources and consequences. Ecological Applications 7, 737-750.
- Volk, N.J., Tidmore, J.W., 1946. Effect of different sources of nitrogen on soil reaction, exchangeable ions, and yields of crops. Soil Science 61, 447-492.
- Wardle, D.A., 1992. A comparative assessment of factors which influence microbial biomass carbon and nitrogen levels in soil. Biological Reviews 67, 321-358.
- Wardle, D.A., Ghani, A., 1995. A critique of the microbial metabolic quotient (qCO2) as a bioindicator of disturbance and ecosystem development. Soil Biology and Biochemistry 27, 1601-1610.
- Wessén, E., Hallin, S., Philippot, L., 2010. Differential responses of bacterial and archaeal groups at high taxonomical ranks to soil management. Soil Biology and Biochemistry 42, 1759-1765.
- Witter, E., Mårtensson, A.M., Garcia, F.V., 1993. Size of the soil microbial biomass in a long-term field experiment as affected by different N-fertilizers and organic manures. Soil Biology and Biochemistry 25, 659-669.
- Wolcott, A.R., Foth, H.D., Davis, J.F., Shickluna, J.C., 1965. Nitrogen carriers: I. Soil effects. Proceedings of the Soil Science Society of America 29, 405-410.
- Yadvinder-Singh, Beauchamp, E.G., 1988. Nitrogen transformations near urea in soil with different water potentials. Canadian Journal of Soil Science 68, 569-576.
- Yadvinder-Singh, Beauchamp, E.G., 1989. Nitrogen transformations near urea in soil: effects of nitrification inhibition, nitrifier activity and liming. Fertilizer Research 18, 201-212.
- Yevdokimov, I., Gattinger, A., Buegger, F., Munch, J.C., Schloter, M., 2008. Changes in microbial community structure in soil as a result of different amounts of nitrogen fertilization. Biology and Fertility of Soils 44, 1103-1106.
- Yevdokimov, I.V., Gattinger, A., Buegger, F., Schloter, M., Munch, J.C., 2012. Changes in the structure and activity of a soil microbial community caused by inorganic nitrogen fertilization. Microbiology 81, 743-749.
- Zhang, H., Wang, B., Xu, M., 2008. Effects of inorganic fertilizer inputs on grain yields and soil properties in a long-term wheatecorn cropping system in south China. Communications in Soil Science and Plant Analysis 39, 1583-1599.
- Zhang, J., Cai, Z., Yang, W., Zhu, T., Yu, Y., Yan, X., Jia, Z., 2012. Long-term field fertilization affects soil nitrogen transformations in a rice-wheat-rotation cropping system. Journal of Plant Nutrition and Soil Science 175, 939-946.
- Zhong, W., Gu, T., Wang, W., Zhang, B., Lin, X., Huang, Q., Shen, W., 2010. The effects of mineral fertilizer and organic manure on soil microbial community and diversity. Plant and Soil 326, 511-522.