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Long-term nitrogen fertilization alters microbial community structure and denitrifier abundance in the deep vadose zone

  • Soils, Sec 5 • Soil and Landscape Ecology • Research Article
  • Published:
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Abstract

Purpose

The excessive use of nitrogen (N) fertilizer in intensive agriculture has increased nitrate leaching into groundwater, but its impacts on N transformation processes and the associated microbial communities in the deep vadose zone remain unclear.

Materials and methods

Soil samples from 0–1050 cm depth were collected from a 20-year field experiment with two N fertilization treatments: 0 (N0) and 600 kg N ha−1 year−1 (N600). Amplicon sequencing and quantitative PCR analyses were performed to profile the vertical distribution of soil microbial communities and denitrification genes.

Results and discussion

The soil microbial community structure and diversity were strongly influenced by soil depth and N fertilization. The 250 cm depth was identified as a threshold depth, as dramatically different microbial communities were found below and above this depth. Quantitative PCR results showed that the absolute abundance of denitrification genes decreased with increasing soil depth.

Conclusion

This study elucidated the profound effects of long-term N input on the composition and diversity of the microbial communities and the abundance of denitrifiers in the deep vadose zone. Our results provide basic information for use in mitigating nitrate leaching by enhancing microbial denitrification in deep vadose zones in intensive agricultural areas.

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References

  • Ascott MJ, Gooddy DC, Wang L, Stuart ME, Lewis MA, Ward RS, Binley AM (2017) Global patterns of nitrate storage in the vadose zone. Nat Commun 8:1416

    Article  CAS  Google Scholar 

  • Banwart SA, Nikolaidis NP, Zhu Y, Peacock CL, Sparks DL (2019) Soil functions: connecting Earth’s critical zone. Annu Rev Earth Pl Sci 47:333–359

    Article  CAS  Google Scholar 

  • Bru D, Ramette A, Saby NPA, Dequiedt S, Ranjard L, Jolivet C, Arrouays D, Philippot L (2011) Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale. ISME J 5:532–542

    Article  CAS  Google Scholar 

  • Cannavo P, Richaume A, Lafolie F (2004) Fate of nitrogen and carbon in the vadose zone: in situ and laboratory measurements of seasonal variations in aerobic respiratory and denitrifying activities. Soil Biol Biochem 36:463–478

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stomabaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  Google Scholar 

  • Chen S, Wang F, Zhang Y, Qin S, Wei S, Wang S, Hu C, Liu B (2018) Organic carbon availability limiting microbial denitrification in the deep vadose zone. Environ Microbiol 20:980–992

    Article  CAS  Google Scholar 

  • Chu H, Sun H, Tripathi BM, Adams JM, Huang R, Zhang Y, Shi Y (2016) Bacterial community dissimilarity between the surface and subsurface soils equals horizontal differences over several kilometers in the western Tibetan Plateau. Environ Microbiol 18:1522–1533

    Article  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  Google Scholar 

  • Eilers KG, Debenport S, Anderson S, Fierer N (2012) Digging deeper to find unique microbial communities: the strong effect of depth on the structure of bacterial and archaeal communities in soil. Soil Biol Biochem 50:58–65

    Article  CAS  Google Scholar 

  • Fierer N (2017) Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol 15:579–590

    Article  CAS  Google Scholar 

  • Guo J, Liu X, Zhang Y, Shen J, Han W, Zhang W, Christie P, Goulding KWT, Vitousek PM, Zhang F (2010) Significant acidification in major Chinese croplands. Science 327:1008–1010

    Article  CAS  Google Scholar 

  • Holden PA, Fierer N (2005) Microbial processes in the vadose zone. Vadose Zone J 4:1–21

    Article  CAS  Google Scholar 

  • Huang T, Ju X, Yang H (2017) Nitrate leaching in a winter wheat-summer maize rotation on a calcareous soil as affected by nitrogen and straw management. Sci Rep 7:42247

    Article  CAS  Google Scholar 

  • Jia X, Zhu Y, Huang L, Wei X, Fang Y, Wu L, Binley A, Shao M (2018) Mineral N stock and nitrate accumulation in the 50 to 200 m profile on the Loess Plateau. Sci Total Environ 633:999–1006

    Article  CAS  Google Scholar 

  • Ju X, Kou C, Zhang F, Christie P (2006) Nitrogen balance and groundwater nitrate contamination: comparison among three intensive cropping systems on the North China Plain. Environ Pollut 143:117–125

    Article  CAS  Google Scholar 

  • Ju X, Xing G, Chen X, Zhang S, Zhang L, Liu X, Cui Z, Yin B, Christie P, Zhu Z, Zhang F (2009) Reducing environmental risk by improving N management in intensive Chinese agricultural systems. Proc Natl Acad Sci USA 106:3041–3046

    Article  CAS  Google Scholar 

  • Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821

    Article  CAS  Google Scholar 

  • Li C, Yan K, Tang L, Jia Z, Li Y (2014) Change in deep soil microbial communities due to long-term fertilization. Soil Biol Biochem 75:264–272

    Article  CAS  Google Scholar 

  • Lu RK (1999) Soil agricultural chemical analysis. China Agricultural Science and Technology Press, Nanjing

    Google Scholar 

  • McCarty GW, Bremner JM (1992) Availability of organic carbon for denitrification of nitrate in subsoils. Biol Fert Soils 14:219–222

    Article  CAS  Google Scholar 

  • Morales SE, Cosart T, Holben WE (2010) Bacterial gene abundances as indicators of greenhouse gas emission in soils. ISME J 4:799–808

    Article  CAS  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) Community Ecology Package. R Package Version 2.5-4. R Core Development Team, Vienna. Available online at: https://github.com/vegandevs/vegan

  • Onyenwoke RU, Brill JA, Farahi K, Wiegel J (2004) Sporulation genes in members of the low G+C Gram-type-positive phylogenetic branch (Firmicutes). Arch Microbiol 182:182–192

    Article  CAS  Google Scholar 

  • Petersen DG, Blazewicz SJ, Firestone M, Herman DJ, Turetsky M, Waldrop M (2012) Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environ Microbiol 14:993–1008

    Article  CAS  Google Scholar 

  • Peterson ME, Curtin D, Thomas S, Clough TJ, Meenken ED (2013) Denitrification in vadose zone material amended with dissolved organic matter from topsoil and subsoil. Soil Biol Biochem 61:96–104

    Article  CAS  Google Scholar 

  • Philippot L, Andert J, Jones CM, Bru D, Hallin S (2011) Importance of denitrifiers lacking the genes encoding the nitrous oxide reductase for N2O emissions from soil. Global Change Biol 17:1497–1504

    Article  Google Scholar 

  • Qin S, Hu C, Clough TJ, Luo J, Oenema O, Zhou S (2017) Irrigation of DOC-rich liquid promotes potential denitrification rate and decreases N2O/(N2O+N2) product ratio in a 0-2 m soil profile. Soil Biol Biochem 106:1–8

    Article  CAS  Google Scholar 

  • Qin S, Wang Y, Hu C, Oenema O, Li X, Zhang Y, Dong W (2012) Yield-scaled N2O emissions in a winter wheat-summer corn double-cropping system. Atmos Environ 55:240–244

    Article  CAS  Google Scholar 

  • Qin W, Zhang X, Chen S, Sun H, Shao L (2018) Crop rotation and N application rate affecting the performance of winter wheat under deficit irrigation. Agr Water Manage 210:330–339

    Article  Google Scholar 

  • Qiu S, Ju X, Ingwersen J, Guo Z, Stange CF, Bisharat R, Streck T, Christie P, Zhang F (2013) Role of carbon substrates added in the transformation of surplus nitrate to organic nitrogen in a Calcareous soil. Pedosphere 23:205–212

    Article  Google Scholar 

  • Qu Z, Wang J, Almoy T, Bakken LR (2014) Excessive use of nitrogen in Chinese agriculture results in high N2O/(N2O+N2) product ratio of denitrification, primarily due to acidification of the soils. Global Change Biol 20:1685–1698

    Article  Google Scholar 

  • Stone MM, Kan JJ, Plante AF (2015) Parent material and vegetation influence bacterial community structure and nitrogen functional genes along deep tropical soil profiles at the Luquillo Critical Zone Observatory. Soil Biol Biochem 80:273–282

    Article  CAS  Google Scholar 

  • Suzuki MT, Taylor LT, DeLong EF (2000) Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5′-nuclease assays. Appl Environ Microb 66:4605–4614

    Article  CAS  Google Scholar 

  • Tang Y, Yu G, Zhang X, Wang Q, Ge J, Liu S (2018) Changes in nitrogen-cycling microbial communities with depth in temperate and subtropical forest soils. Appl Soil Ecol 124:218–228

    Article  Google Scholar 

  • van Egmond K, Bresser T, Bouwman L (2002) The European nitrogen case. Ambio 31:72–78

    Article  Google Scholar 

  • Wang F, Chen S, Wang Y, Zhang Y, Hu C, Liu B (2018) Long-term nitrogen fertilization elevates the activity and abundance of nitrifying and denitrifying microbial communities in an upland soil: implications for nitrogen loss from intensive agricultural systems. Front Microbiol 9:2424

    Article  Google Scholar 

  • Wang Y, Hu C, Ming H, Zhang Y, Li X, Dong W, Oenema O (2013) Concentration profiles of CH4, CO2 and N2O in soils of a wheat-maize rotation ecosystem in North China Plain, measured weekly over a whole year. Agr Ecosyst Environ 164:260–272

    Article  CAS  Google Scholar 

  • Wang S, Wei S, Liang H, Zheng W, Li X, Hu C, Currell MJ, Zhou F, Min L (2019) Nitrogen stock and leaching rates in a thick vadose zone below areas of long-term nitrogen fertilizer application in the North China Plain: a future groundwater quality threat. J Hydrol 576:28–40

    Article  CAS  Google Scholar 

  • Wickham H, Chang W, Pedersen TL, Takahashi K, Wilke C, Woo K, Yutani H (2019) Create elegant data visualizations using the grammar of graphics. R package version 3.2.1, http://ggplot2.tidyverse.org

  • Wu Y, Li Y, Fu X, Liu X, Shen J, Wang Y, Wu J (2016) Three-dimensional spatial variability in soil microorganisms of nitrification and denitrification at a row-transect scale in a tea field. Soil Biol Biochem 103:452–463

    Article  CAS  Google Scholar 

  • Yasir M, Angelakis E, Bibi F, Azhar EI, Bachar D, Lagier JC, Gaborit B, Hassan AM, Jiman-Fatani AA, Alshali KZ, Robert C, Dutour A, Raoult D (2015) Comparison of the gut microbiota of people in France and Saudi Arabia. Nutr Diab 5:e153

    Article  CAS  Google Scholar 

  • Yuan H, Qin S, Dong W, Hu C, Manevski K, Li X (2017) Denitrification rates and controlling factors for accumulated nitrate in the 0-12 m intensive farmlands: a case study in the North China Plain. Pedosphere. S1002016017604727

  • Zhang M, Dong B, Qiao Y, Shi C, Yang H, Wang Y, Liu M (2018) Yield and water use responses of winter wheat to irrigation and nitrogen application in the North China Plain. J Integr Agr 17:1194–1206

    Article  Google Scholar 

  • Zhou J, Gu B, Schlesinger WH, Ju X (2016) Significant accumulation of nitrate in Chinese semi-humid croplands. Sci Rep 6:25088

    Article  CAS  Google Scholar 

  • Zhou W, Ma YC, Well R, Wang H, Yan X (2018) Denitrification in shallow groundwater below different arable land systems in a high nitrogen-loading region. J Geophys Res-Biogeo 123:991–1004

    Article  CAS  Google Scholar 

  • Zhu G, Wang S, Li Y, Zhuang L, Zhao S, Wang C, Kuypers MMM, Jetten MSM, Zhu Y (2018) Microbial pathways for nitrogen loss in an upland soil. Environ Microbiol 20:1723–1738

    Article  CAS  Google Scholar 

  • Zhu A, Zhang J, Zhao B, Cheng Z, Li L (2005) Water balance and nitrate leaching losses under intensive crop production with Ochric Aquic Cambosols in North China Plain. Environ Int 31:904–912

    Article  Google Scholar 

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Acknowledgements

We would like to thank Prof. Yongguan Zhu, Prof. Zheng Chen, Prof. Feng Zhu, and Dr. Zhaohai Bai for their constructive suggestions on this manuscript. We would also like to thank the students and staff that assisted us in taking the soil samples.

Funding

This work was supported by the National Key Research and Development Program of China (2016YFD0800100, 2016YFD0200307), the Key Program of the National Natural Science Foundation of China (41930865, 41530859), and the National Natural Science Foundation of China (41877425, 41807058).

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Authors and Affiliations

  1. Key Laboratory of Agricultural Water Resources, Hebei Key Laboratory of Soil Ecology, Center for Agricultural Resources Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Shijiazhuang, 050021, China

    Fenghua Wang, Shuaimin Chen, Ruibo Sun, Yuming Zhang, Shiqin Wang, Chunsheng Hu & Binbin Liu

  2. State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, 100085, China

    Fenghua Wang

  3. University of Chinese Academy of Sciences, Beijing, 100039, China

    Shuaimin Chen

  4. Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    Shuping Qin

  5. Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, 3010, Australia

    Hangwei Hu

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  1. Fenghua Wang
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Correspondence to Hangwei Hu or Binbin Liu.

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Wang, F., Chen, S., Qin, S. et al. Long-term nitrogen fertilization alters microbial community structure and denitrifier abundance in the deep vadose zone. J Soils Sediments 21, 2394–2403 (2021). https://doi.org/10.1007/s11368-021-02931-0

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  • DOI: https://doi.org/10.1007/s11368-021-02931-0

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