Functional Soil Organic Matter Fractions, Microbial Community, and Enzyme Activities in a Mollisol Under 35 Years Manure and Mineral Fertilization

  • Fan Yang
  • Jing TianEmail author
  • Huajun Fang
  • Yang Gao
  • Minggang Xu
  • Yilai Lou
  • Baoku Zhou
  • Yakov Kuzyakov
Research Article


Fertilization is a worldwide practice to maintain and increase crop productivity and improve soil quality in agricultural ecosystems. The interactive mechanisms of long-term fertilization affecting the functional soil organic matter (SOM) fractions, microbial community, and enzyme activities are unclear. We investigated the effects of manure and mineral fertilization on six SOM fractions (non-protected, physically, chemically, biochemically, physical-chemically, and physical-biochemically protected), microbial community structure, and enzyme activities based on a 35-year fertilization experiment. The combined application of manure and mineral fertilizers (NPKM) increased the soil organic carbon (SOC) and total nitrogen (TN) in the biochemically (28.6–43.9%) and physically (108–229%) protected fractions, compared to their content in the unfertilized soil (CK). The total phospholipid fatty acid content, Gram(−) bacteria, and actinomycetes, as well as the activities of α-1,4-glucosidase, β-1,4-N-acetylglucosaminidase, β-1,4-xylosidase, and cellobiohydrolase were highest under NPKM fertilization. The protected SOM fractions (physical, biochemical, physical-chemical, and physical-biochemical) were closely related to microbial community composition (accounting for 67.6% of the variance). Bacteria were sensitive to changes in the physically and biochemically protected fractions, whereas fungi responded more to the changes in the chemically protected fraction. In summary, long-term mineral and organic fertilization has a strong effect on microbial communities and activities through the changes in the functional SOM fractions.


Long-term fertilization Soil organic matter fractions Soil aggregation Microbial community composition Enzyme activities 



We thank the Editor and the anonymous reviewers for their valuable comments that helped us to greatly improve the manuscript.


This study is financially supported by the National Natural Science Foundation of China (Grant No. 41571130041; 31770560) and the Major Program of the National Natural Science Foundation of China (Grant No. 2017YFA0604803). The publication was supported by the Government Program of Competitive Growth of Kazan Federal University and with the support of the “RUDN University program 5-100.”


  1. Balser TC, Firestone MK (2005) Linking microbial community composition and soil processes in a California annual grassland and mixed-conifer forest. Biogeochemistry. 73:395–415CrossRefGoogle Scholar
  2. Basanta R, de Varennes A, Diaz-Ravina M (2017) Microbial community structure and biomass of a mine soil with different organic and inorganic treatments and native plants. J Soil Sci Plant Nutr 17:839–852CrossRefGoogle Scholar
  3. Bird JA, Herman DJ, Firestone MK (2011) Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil. Soil Biol Biochem 43:718–725CrossRefGoogle Scholar
  4. Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234CrossRefGoogle Scholar
  5. Cookson WR, Abaye DA, Marschner P, Murphy DV, Stockdale EA, Goulding KWT (2005) The contribution of soil organic matter fractions to carbon and nitrogen mineralization and microbial community size and structure. Soil Biol Biochem 37:1726–1737CrossRefGoogle Scholar
  6. Cusack DF, Silver WL, Torn MS, Burton SD, Firestone MK (2011) Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests. Ecology. 92:621–632CrossRefGoogle Scholar
  7. Ding X, Han X, Liang Y, Qiao Y, Li L, Li N (2012) Changes in soil organic carbon pools after 10 years of continuous manuring combined with chemical fertilizer in a Mollisol in China. Soil Tillage Res 122:36–41CrossRefGoogle Scholar
  8. Dong W, Zhang X, Dai X, Fu X, Yang F, Liu X, Sun X, Wen X, Schaeffer S (2014) Changes in soil microbial community composition in response to fertilization of paddy soils in subtropical China. Appl Soil Ecol 84:140–147CrossRefGoogle Scholar
  9. Frostegård A, Tunlid A, Baath E (1991) Microbial biomass measured as total lipid phosphate in soils of different organic content. J Microbiol Methods 14:151–163CrossRefGoogle Scholar
  10. Frostegård A, Bååth E, Tunlio A (1993) Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis. Soil Biol Biochem 25:723–730CrossRefGoogle Scholar
  11. Guillaume T, Maranguit D, Murtilaksono K, Kuzyakov Y (2016) Sensitivity and resistance of soil fertility indicators to land-use changes: new concept and examples from conversion of Indonesian rainforest to plantations. Ecol Indic 67:49–57CrossRefGoogle Scholar
  12. Hai L, Li XG, Li FM, Suo DR, Guggenberger G (2010) Long-term fertilization and manuring effects on physically-separated soil organic matter pools under a wheat–wheat–maize cropping system in an arid region of China. Soil Biol Biochem 42:253–259CrossRefGoogle Scholar
  13. Joachim R, Meike O (2002) Fractions of particulate organic matter in soils depending upon farmyard manure and mineral fertilization. Proc.14th IFOAM Organic World Congress. Victoria, Canada, p 25Google Scholar
  14. Li J, Cooper JM, Lin ZA, Li YT, Yang XD, Zhao BQ (2015) Soil microbial community structure and function are significantly affected by long-term organic and mineral fertilization regimes in the North China Plain. Appl Soil Ecol 96:75–87CrossRefGoogle Scholar
  15. Li XG, Jia B, Lv J, Ma Q, Kuzyakov Y, Li F (2017) Nitrogen fertilization decreases the decomposition of soil organic matter and plant residues in planted soils. Soil Biol Biochem 112:47–55CrossRefGoogle Scholar
  16. Lu Y, Abraham WR, Conrad R (2007) Spatial variation of active microbiota in the rice rhizosphere revealed by in situ stable isotope probing of phospholipid fatty acids. Environ Microbiol 9:474–481CrossRefGoogle Scholar
  17. Plante AF, Conant RT, Stewart CE, Paustian K, Six J (2006a) Impact of soil texture on the distribution of soil organic matter in physical and chemical fractions. Soil Sci Soc Am J 70:287–296CrossRefGoogle Scholar
  18. Plante AF, Conant RT, Paul EA, Paustian K, Six J (2006b) Acid hydrolysis of easily dispersed and microaggregate-derived silt-and clay-sized fractions to isolate resistant soil organic matter. Eur J Soil Sci 57:456–467CrossRefGoogle Scholar
  19. Reicosky DC, Evans SD, Cambardella CA, Armaras RR, Wilts AR, Huggins DR (2002) Continuous corn with moldboard tillage: residue and fertility effects on soil carbon. J Soil Water Conserv 57:277–284Google Scholar
  20. Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315CrossRefGoogle Scholar
  21. Six J, Elliot ET, Paustian K (2000) Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biol Biochem 32:2099–2103CrossRefGoogle Scholar
  22. Six J, Conant RT, Paul EA, Paustian K (2002) Stabilization mechanisms of soil organic matter: implications for C-saturation of soils. Plant Soil 241:155–176CrossRefGoogle Scholar
  23. Sobczak WV, Hedin KO, Klug MJ (1998) Relationships between bacterial productivity and organic carbon at a soil-stream interface. Hydrobiologia 386:45–53CrossRefGoogle Scholar
  24. Solomon D, Fritzsche F, Tekalign M, Lehmann J, Zech W (2002) Soil organic matter dynamics in the sub-humid Ethiopian highlands: evidence from natural 13C abundance and particle-size fractionation. Soil Sci Soc Am J 66:969–978CrossRefGoogle Scholar
  25. Stevenson FJ (1994) Humus chemistry: genesis, composition. Reactions. John Wiley & Sons, New York, p 496Google Scholar
  26. Stewart CE, Plante AF, Paustian KP, Conant RT, Six J (2008) Soil carbon saturation: linking concept and measurable carbon pools. Soil Sci Soc Am J 72:379–392CrossRefGoogle Scholar
  27. Stewart CE, Paustian K, Conant RT, Plante AF, Six J (2009) Soil carbon saturation: implications for measurable carbon pool dynamics in long-term incubations. Soil Biol Biochem 41:357–366CrossRefGoogle Scholar
  28. Tang H, Xiao X, Tang W, Lin Y, Wang K, Yang G (2014) Effects of winter cover crops residue returning on soil enzyme activities and soil microbial community in double-cropping rice fields. PLoS One 9:e100443CrossRefGoogle Scholar
  29. Tian J, Lou Y, Gao Y, Fang H, Liu S, Xu M, Blagodatskaya E, Kuzyakov Y (2017) Response of soil organic matter fractions and composition of microbial community to long-term organic and mineral fertilization. Biol Fertil Soils 53:523–532CrossRefGoogle Scholar
  30. Wang Y, Hu N, Xu M, Li Z, Lou Y, Chen Y, Wu C, Wang ZL (2015) 23-year manure and fertilizer application increases soil organic carbon sequestration of a rice-barley cropping system. Biol Fertil Soils 51:583–591CrossRefGoogle Scholar
  31. Williams A, Börjesson G, Hedlund K (2013) The effects of 55 years of different mineral fertiliser regimes on soil properties and microbial community composition. Soil Biol Biochem 67:41–46CrossRefGoogle Scholar
  32. Yin YF, Cai ZC (2006) Equilibrium of organic matter in heavy fraction for three long-term experimental field soils in China. Pedosphere. 16:177–184CrossRefGoogle Scholar
  33. Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccha- rides in the characterisation of microbial communities in soil: a review. Biol Fertil Soils 29:111–129CrossRefGoogle Scholar
  34. Zhang H, Ding W, Yu H, He X (2015) Linking organic carbon accumulation to microbial community dynamics in a sandy loam soil: result of 20 years compost and mineral fertilizers repeated application experiment. Biol Fertil Soils 51:137–150CrossRefGoogle Scholar
  35. Zhao S, Li K, Zhou W, Qiu S, Huang S, He P (2016) Changes in soil microbial community, enzyme activities and organic matter fractions under long-term straw return in north-Central China. Agric Ecosyst Environ 216:82–88CrossRefGoogle Scholar

Copyright information

© Sociedad Chilena de la Ciencia del Suelo 2019

Authors and Affiliations

  • Fan Yang
    • 1
    • 2
    • 3
  • Jing Tian
    • 1
    • 2
    Email author
  • Huajun Fang
    • 2
  • Yang Gao
    • 2
  • Minggang Xu
    • 4
  • Yilai Lou
    • 5
  • Baoku Zhou
    • 6
  • Yakov Kuzyakov
    • 7
    • 8
    • 9
  1. 1.College of Resources and Environmental Sciences; National Academy of Agriculture Green Development; Key Laboratory of Plant-Soil Interactions, Ministry of Education China Agricultural UniversityBeijingChina
  2. 2.Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research Chinese Academy of SciencesBeijingChina
  3. 3.State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Institute of Soil and Water ConservationChinese Academy of Sciences and Ministry of Water ResourcesYanglingChina
  4. 4.National Engineering Laboratory for Improving Quality of Arable Land, Institute of Agricultural Resources and Regional PlanningChinese Academy of Agricultural SciencesBeijingChina
  5. 5.Institute of Environment and Sustainable Development in AgricultureChinese Academy of Agricultural SciencesBeijingChina
  6. 6.Institute of Soil Fertilizer and Environment ResourcesHeilongjiang Academy of Agricultural SciencesHaerbinChina
  7. 7.Department of Soil Science of Temperate Ecosystems, Department of Agricultural Soil ScienceUniversity of GöttingenGöttingenGermany
  8. 8.Institute of Environmental SciencesKazan Federal UniversityKazanRussia
  9. 9.Agro-Technological InstituteRUDN UniversityMoscowRussia

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