Journal of Soils and Sediments

, Volume 18, Issue 5, pp 1853–1864 | Cite as

Soil pH rather than nutrients drive changes in microbial community following long-term fertilization in acidic Ultisols of southern China

  • Jia Liu
  • Ming Liu
  • Meng Wu
  • Chunyu Jiang
  • Xiaofen Chen
  • Zejiang Cai
  • Boren Wang
  • Jie Zhang
  • Taolin Zhang
  • Zhongpei LiEmail author
Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article



Long-term intensive cultivation and heavy fertilization improve the nutritional conditions in acidic Ultisols, but also sharply accelerate soil acidification. However, the impact of such dramatic environmental changes on soil microorganisms is unclear. The aims of this work were to investigate the responses of microbial community composition and metabolic function to long-term fertilization, and to determine the key factors that primarily drive microbial changes in acidic Ultisols.

Materials and methods

A long-term fertilization experiment under a winter wheat–summer maize rotation was established in 1990 in acidic Ultisols of southern China. Soils were collected from four treatments in June 2014: (1) non-fertilization control (CK); (2) only N fertilization (N); (3) N, P, and K fertilization (NPK); and (4) NPK plus manure (NPKM; 70% of total N obtained from manure). The amount of N used in all N treatments was 300 kg N ha−1 year−1. The soil pH, cation exchange capacity (CEC), soil organic carbon (SOC), total nitrogen (TN), phosphorus (TP) and potassium (TK), available nitrogen (AN), phosphorus (AP), and potassium (AK) were measured. Soil microbial community composition and metabolic function were determined by phospholipid fatty acids analysis (PLFA) and community-level physiological profile (CLPP) method, respectively.

Results and discussion

Compared with CK, NPKM significantly increased total PLFA biomass and average well color development (AWCD); NPK increased total PLFA biomass by 2.2 times, but its AWCD was not significantly different from CK, indicating that microbial metabolic efficiency in NPK decreased. N decreased total PLFA biomass by 27.9%, while almost completely inhibiting metabolic activity. NPKM maintained microbial functional diversity indexes at similar levels as CK, while NPK and N significantly decreased microbial functional diversity indexes. Redundancy analysis (RDA) revealed that soil microbial community composition and metabolic pattern were more stably maintained by application of manure compared to chemical fertilizers. Soil pH showed the primary effect on microbial community composition, metabolic activity, and functional diversity indexes.


This research demonstrated that the negative effects of Ultisol acidification induced by long-term application of chemical N fertilizer on microorganisms overwhelmed the positive effects of soil nutrition improvement. The inhibiting effect of serious acidification on microbial metabolic function was stronger than that on community composition. Microorganisms live in a low active metabolic state to resist serious Ultisols acidification. Therefore, fertilization in acidic Ultisols should be based on the premise of preventing soil further acidification.


Acidification CLPP Long-term fertilization PLFA Ultisols 



This study is supported by the National Basic Research Program (973 Program) of China (No. 2014CB441003) and the National Natural Science Foundation of China (Nos. 41661052 and 31660599). In addition, we thank the anonymous reviewers and editors for their helpful comments regarding the manuscript.

Supplementary material

11368_2018_1934_MOESM1_ESM.doc (62 kb)
ESM 1 (DOC 62 kb)


  1. Abdulahaal BM, Li JY, Xu CY, Mehmood K, Xu RK (2017) Determination of critical pH and Al concentration of acidic Ultisols for wheat and canola crops. Solid Earth 8:149–159CrossRefGoogle Scholar
  2. Allison SD, Martiny JB (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci U S A 105(Supplement 1):11512–11519. CrossRefGoogle Scholar
  3. Berg G (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biot 84(1):11–18. CrossRefGoogle Scholar
  4. Birgander J, Reischke S, Jones DL, Rousk J (2013) Temperature adaptation of bacterial growth and 14C-glucose mineralisation in a laboratory study. Soil Biol Biochem 65:294–303. CrossRefGoogle Scholar
  5. Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89:2623–2632CrossRefGoogle Scholar
  6. Buyer JS, Teasdale JR, Roberts DP, Zasada IA, Maul JE (2010) Factors affecting soil microbial community structure in tomato cropping systems. Soil Biol Biochem 42(5):831–841. CrossRefGoogle Scholar
  7. Cai ZJ, Wang BR, Xu MG, Zhang HM, He XH, Zhang L, Gao SD (2015) Intensified soil acidification from chemical N fertilization and prevention by manure in an 18-year field experiment in the red soil of southern China. J Soils Sediments 15(2):260–270. CrossRefGoogle Scholar
  8. Cai ZJ, Wang BR, Xu MG, Zhang HM, Zhang L, Gao SD (2014) Nitrification and acidification from urea application in red soil (Ferralic Cambisol) after different long-term fertilization treatments. J Soils Sediments 14(9):1526–1536. CrossRefGoogle Scholar
  9. Chen L, Xun WB, Sun L, Zhang N, Shen QR, Zhang RF (2014) Effect of different long-term fertilization regimes on the viral community in an agricultural soil of southern China. Eur Soil Bio 62:121–126. CrossRefGoogle Scholar
  10. Chen XF, Li ZP, Liu M, Jiang CY, Che YP (2015) Microbial community and functional diversity associated with different aggregate fractions of a paddy soil fertilized with organic manure and/or NPK fertilizer for 20 years. J Soils Sediments 15(2):292–301. CrossRefGoogle Scholar
  11. Dong WY, Zhang XY, Wang HM, Dai XQ, Sun XM, Qiu WW, Yang FT (2012) Effect of different fertilizer application on the soil fertility of paddy soils in red soil region of southern China. PLoS One 7(9):e44504. CrossRefGoogle Scholar
  12. Dorea CC, Clarke BA (2008) Effect of aluminium on microbial respiration. Water Air Soil Pollut 189(1-4):353–358. CrossRefGoogle Scholar
  13. Fanin N, Hättenschwiler S, Fromin N (2014) Litter fingerprint on microbial biomass, activity, and community structure in the underlying soil. Plant Soil 379:79–91CrossRefGoogle Scholar
  14. Fierer N, Schimel JP, Holden PA (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35(1):167–176. CrossRefGoogle Scholar
  15. Garland JL (1996) Analytical approaches to the characterization of samples of microbial communities using patterns of potential C source utilization. Soil Biol Biochem 28(2):213–221. CrossRefGoogle Scholar
  16. Gerke J (2010) Humic (organic matter)-Al (Fe)-phosphate complexes: an underestimated phosphate form in soils and source of plant-available phosphate. Soil Sci 175(9):417–425. CrossRefGoogle Scholar
  17. Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding KW, Vitousek PM, Zhang FS (2010) Significant acidification in major Chinese croplands. Science 327(5968):1008–1010. CrossRefGoogle Scholar
  18. Hammesfahr U, Heuer H, Manzke B, Smalla K, Thielebruhn S (2008) Impact of the antibiotic sulfadiazine and pig manure on the microbial community structure in agricultural soils. Soil Biol Biochem 40:1583–1591CrossRefGoogle Scholar
  19. Hartman WH, Richardson CJ, Vilgalys R, Bruland GL (2008) Environmental and anthropogenic controls over bacterial communities in wetland soils. Proc Natl Acad Sci U S A 105(46):17842–17847. CrossRefGoogle Scholar
  20. Hu XJ, Liu JJ, Wei D, Zhu P, Cui XA, Zhou BK, Chen XL, Jin J, Liu XB, Wang GH (2017) Effects of over 30-year of different fertilization regimes on fungal community compositions in the black soils of northeast China. Agric Ecosyst Environ 248:113–122. CrossRefGoogle Scholar
  21. Huang R, Wu YC, Zhang JB, Zhong WH, Jia ZJ, Cai ZC (2012) Nitrification activity and putative ammonia-oxidizing archaea in acidic red soils. J Soils Sediments 12(3):420–428. CrossRefGoogle Scholar
  22. Huang S, Zhang W, Yu X, Huang QR (2010) Effects of long-term fertilization on corn productivity and its sustainability in an Ultisol of southern China. Agric Ecosyst Environ 138(1-2):44–50. CrossRefGoogle Scholar
  23. Kušlienė G, Rasmussen J, Kuzyakov Y, Eriksen J (2014) Medium-term response of microbial community to rhizodeposits of white clover and ryegrass and tracing of active processes induced by 13C and 15N labelled exudates. Soil Biol Biochem 76:22–33. CrossRefGoogle Scholar
  24. Lauber CL, Hamady M, Knight R, Fierer NP (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microb 75(15):5111–5120. CrossRefGoogle Scholar
  25. Legendre P, Gallagher E (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129(2):271–280. CrossRefGoogle Scholar
  26. Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9(2):119–130. CrossRefGoogle Scholar
  27. Li WT, Liu M, Jiang CY, Wu M, Chen XF, Ma XY, Li ZP (2017) Changes in soil aggregate- associated enzyme activities and nutrients under long-term chemical fertilizer applications in a phosphorus-limited paddy soil. Soil Use Manage 33(1):25–33. CrossRefGoogle Scholar
  28. Ma XY, Liu M, Li ZP (2015) Changes in microbial properties and community composition in acid soils receiving wastewater from concentrated animal farming operations. Appl Soil Ecol 90:11–17CrossRefGoogle Scholar
  29. Ma XY, Liu M, Li ZP (2016) Shifts in microbial biomass and community composition in subtropical paddy soils under a gradient of manure amendment. Biol Fert. Soils 52:775–787Google Scholar
  30. National Bureau of Statistics of China (2016) China statistical yearbook. China Statistics Press, BeijingGoogle Scholar
  31. Pansu M, Gautheyrou J (2006) Handbook of soil analysis: mineralogical, organic and inorganic methods. Springer, Berlin Heidelberg, Berlin. CrossRefGoogle Scholar
  32. Peng CJ, Lai SS, Luo XS, Lu JW, Huang QY, Chen WL (2016) Effects of long term rice straw application on the microbial communities of rapeseed rhizosphere in a paddy-upland rotation system. Sci Total Environ 557-558:231–239. CrossRefGoogle Scholar
  33. Rittershaus ESC, Baek SH, Sassetti CM (2013) The normalcy of dormancy: common themes in microbial quiescence. Cell Host Microbe 13(6):643–651. CrossRefGoogle Scholar
  34. Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4(10):1340–1351. CrossRefGoogle Scholar
  35. Rukshana F, Butterly CR, Xu JM, Baldock JA, Tang CX (2014) Organic anion-to-acid ratio influences pH change of soils differing in initial pH. J Soils Sediments 14(2):407–414. CrossRefGoogle Scholar
  36. Shen CC, Xiong JB, Zhang HY, Feng YZ, Lin XG, Li XY, Liang WJ, Chu HY (2013) Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol Biochem 57:204–211. CrossRefGoogle Scholar
  37. Sistla SA, Schimel JP (2012) Stoichiometric flexibility as a regulator of carbon and nutrient cycling in terrestrial ecosystems under change. New Phytol 196(1):68–78. CrossRefGoogle Scholar
  38. Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70(2):555–569. CrossRefGoogle Scholar
  39. Sun RB, Zhang XX, Guo XS, Wang DZ, Chu HY (2015) Bacterial diversity in soils subjected to long-term chemical fertilization can be more stably maintained with the addition of livestock manure than wheat straw. Soil Biol Biochem 88:9–18. CrossRefGoogle Scholar
  40. Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11(10):1111–1120. CrossRefGoogle Scholar
  41. Ulrich B (1986) Natural and anthropogenic components of soil acidification. J Plant Nutr Soil Sci 149:702–717Google Scholar
  42. Waldrop M, Firestone M (2004) Microbial community utilization of recalcitrant and simple carbon compounds: impact of oak-woodland plant communities. Oecologia 138(2):275–284. CrossRefGoogle Scholar
  43. Xiang XJ, He D, He JS, Myrold DD, Chu HY (2017) Ammonia-oxidizing bacteria rather than archaea respond to short-term urea amendment in an alpine grassland. Soil Biol Biochem 107:218–225. CrossRefGoogle Scholar
  44. Xun WB, Huang T, Zhao J, Ran W, Wang BR, Shen QR, Zhang RF (2015) Environmental conditions rather than microbial inoculum composition determine the bacterial composition, microbial biomass and enzymatic activity of reconstructed soil microbial communities. Soil Biol Biochem 90:10–18. CrossRefGoogle Scholar
  45. Yuan JH, Xu RK, Qian W, Wang RH (2011) Comparison of the ameliorating effects on an acidic ultisol between four crop straws and their biochars. J Soils Sediments 11(5):741–750. CrossRefGoogle Scholar
  46. Yue XL, Zhang JG, Shi AD, Yao SH, Zhang B (2016) Manure substitution of mineral fertilizers increased functional stability through changing structure and physiology of microbial communities. Eur J Soil Biol 77:34–43. CrossRefGoogle Scholar
  47. Zelles L (1997) Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere 35(1-2):275–294. CrossRefGoogle Scholar
  48. Zhang Q, Zhou W, Liang GQ, Sun JW, Wang XB, He P (2015) Distribution of soil nutrients, extracellular enzyme activities and microbial communities across particle-size fractions in a long-term fertilizer experiment. Appl Soil Ecol 94:59–71. CrossRefGoogle Scholar
  49. Zhang XB, Wu LH, Sun N, Ding XS, Li JW, Wang BR, Li DC (2014) Soil CO2 and N2O emissions in maize growing season under different fertilizer regimes in an upland red soil region of South China. J Integr Agr 13(3):604–614. CrossRefGoogle Scholar
  50. Zhong WH, Gu T, Wei W, Zhang B, Lin XG, Huang QR, Shen WS (2010) The effects of mineral fertilizer and organic manure on soil microbial community and diversity. Plant Soil 326(1-2):511–522. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Jia Liu
    • 1
    • 2
    • 3
  • Ming Liu
    • 1
  • Meng Wu
    • 1
  • Chunyu Jiang
    • 1
  • Xiaofen Chen
    • 1
  • Zejiang Cai
    • 4
  • Boren Wang
    • 4
  • Jie Zhang
    • 5
  • Taolin Zhang
    • 1
    • 2
  • Zhongpei Li
    • 1
    • 2
    Email author
  1. 1.State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil ScienceChinese Academy of SciencesNanjingChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Soil and Fertilizer & Resources and Environment InstituteJiangxi Academy of Agricultural SciencesNanchangChina
  4. 4.Ministry of Agriculture Key Laboratory of Crop Nutrition and Fertilization, Institute of Agricultural Resources and Regional PlanningChinese Academy of Agricultural SciencesBeijingChina
  5. 5.Nanchang Institute of TechnologyNanchangChina

Personalised recommendations