Influence of Biochar Addition on the Denitrification Process and N2O Emission in Cd-Contaminated Soil

  • Guanhong Chen
  • Zhirong Zhang
  • Zhiyuan Zhang
  • Renduo Zhang
Article

Abstract

The aim of this study was to investigate the effect of biochar addition on the denitrification process and N2O emission in Cd-contaminated soil. Four different biochars, i.e., dairy manure and rice straw pyrolyzed at 350 and 550 °C, respectively, were added into a Cd-contaminated soil and incubation experiments were conducted for 8 weeks. Results showed that Cd had an inhibitory effect on denitrifying reductase enzymes and reduced the abundance of functional genes. On the contrary, amendment with the biochars increased denitrifying enzyme activity and gene abundance, and thus, enhanced the denitrification process. Labile carbon (C) in the biochar-amended soil, which was calculated based on the two-pool exponential model, was the key factor to facilitate this process. As a less important factor, elevated soil pH by biochar addition also increased denitrifying activity as well as the nosZ abundance. Decrease of Cd bioavailability by the biochar addition was beneficial to the denitrification process. Addition of the biochars with higher amount of NO3 -N, especially the rice straw-derived biochars, increased cumulative N2O emission by more than ten times relative to the Cd-contaminated soil. With the great amount of labile C and NO3 -N, the treatment of biochars prepared at 350 °C released the larger amount of CO2 and N2O than other treatments. The biochar addition could totally release the heavy metal stress and restore the Cd-contaminated soil in terms of bacterial community.

Keywords

Biochar Cd-contaminated soil Denitrification process N2O emission 

Notes

Acknowledgements

This study was partly supported by grant from the Chinese National Natural Science Foundation (No. 41471181).

References

  1. Adriano, D. C. (2001). Trace elements in the terrestrial environments: biogeochemistry, bioavailability, and risks of heavy metals. New York: Springer.CrossRefGoogle Scholar
  2. Ameloot, N., De Neve, S., Jegajeevagan, K., Yildiz, G., Buchan, D., Funkuin, Y. N., Prins, W., Bouckaert, L., & Sleutel, S. (2013). Short-term CO2 and N2O emissions and microbial properties of biochar amended sandy loam soils. Soil Biology & Biochemistry, 57, 401–410.CrossRefGoogle Scholar
  3. Ameloot, N., Maenhout, P., De Neve, S., & Sleutel, S. (2016). Biochar-induced N2O emission reductions after field incorporation in a loam soil. Geoderma, 267, 10–16.CrossRefGoogle Scholar
  4. Baggs, E. M., Rees, R. M., Smith, K. A., & Vinten, A. J. A. (2006). Nitrous oxide emission from soils after incorporating crop residues. Soil Use and Management, 16(2), 82–87.CrossRefGoogle Scholar
  5. Baggs, E. M., Smales, C. L., & Bateman, E. J. (2010). Changing pH shifts the microbial source as well as the magnitude of N2O emission from soil. Biology and Fertility of Soils, 46(8), 793–805.CrossRefGoogle Scholar
  6. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Pena, A. G., Goodrich, J. K., & Gordon, J. I. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5), 335–336.CrossRefGoogle Scholar
  7. Cayuela, M. L., Jeffery, S., & van Zwieten, L. (2015). The molar H:Corg ratio of biochar is a key factor in mitigating N2O emissions from soil. Agriculture, Ecosystems & Environment, 202, 135–138.CrossRefGoogle Scholar
  8. Cayuela, M.L., Oenema, O., Kuikman, P.J., Bakker, R.R., & Van Groenigen, J. W. (2010). Bioenergy by-products as soil amendments? Implications for carbon sequestration and greenhouse gas emissions. GCB Bioenergy 2: 201–213.Google Scholar
  9. Cayuela, M. L., van Zwieten, L., Singh, B. P., Jeffery, S., Roig, A., & Sánchez-Monedero, M. A. (2014). Biochar’s role in mitigating soil nitrous oxide emissions: a review and meta-analysis. Agriculture, Ecosystems & Environment, 191, 5–16.CrossRefGoogle Scholar
  10. Cui, L., Yan, J., & Yang, Y. (2013). Influence of biochar on microbial activities of heavy metals contaminated paddy fields. BioResources, 8, 5536–5548.Google Scholar
  11. Dong, D., Feng, Q., McGrouther, K., Yang, M., Wang, H., & Wu, W. (2014). Effects of biochar amendment on rice growth and nitrogen retention in a waterlogged paddy field. Journal of Soils and Sediments, 15, 153–162.CrossRefGoogle Scholar
  12. Ducey, T. F., Ippolito, J. A., Cantrell, K. B., Novak, J. M., & Lentz, R. D. (2013). Addition of activated switchgrass biochar to an aridic subsoil increases microbial nitrogen cycling gene abundances. Applied Soil Ecology, 65, 65–72.CrossRefGoogle Scholar
  13. Gao, S., Zhao, M., Chen, Y., Yu, M., & Ruan, W. (2015). Tolerance response to in situ ammonia stress in a pilot-scale anaerobic digestion reactor for alleviating ammonia inhibition. Bioresource Technology, 198, 372–379.CrossRefGoogle Scholar
  14. Garau, G., Castaldi, P., Santona, L., Deiana, P., & Melis, P. (2007). Influence of red mud, zeolite and lime on heavy metal immobilization, culturable heterotrophic microbial populations and enzyme activities in a contaminated soil. Geoderma, 142(1-2), 47–57.CrossRefGoogle Scholar
  15. Harter, J., Krause, H. M., Schuettler, S., Ruser, R., Fromme, M., Scholten, T., Kappler, A., & Behrens, S. (2014). Linking N2O emissions from biochar-amended soil to the structure and function of the N-cycling microbial community. ISME Journal, 8(3), 660–674.CrossRefGoogle Scholar
  16. Helder, W., & De Vries, R. T. P. (1979). An automatic phenol-hypochlorite method for the determination of ammonia in sea-and brackish waters. Netherlands Journal of Sea Research, 13(1), 154–160.CrossRefGoogle Scholar
  17. Huang, C., Li, Z., Chen, F., Liu, Q., Zhao, Y., Zhou, J., & Wang, A. (2015). Microbial community structure and function in response to the shift of sulfide/nitrate loading ratio during the denitrifying sulfide removal process. Bioresource Technology, 197, 227–234.CrossRefGoogle Scholar
  18. Jones, D. L., Murphy, D. V., Khalid, M., Ahmad, W., Edwards-Jones, G., & DeLuca, T. H. (2011). Short-term biochar-induced increase in soil CO2 release is both biotically and abiotically mediated. Soil Biology & Biochemistry, 43(8), 1723–1731.CrossRefGoogle Scholar
  19. Khodadad, C. L. M., Zimmerman, A. R., Green, S. J., Uthandi, S., & Foster, J. S. (2011). Taxa-specific changes in soil microbial community composition induced by pyrogenic carbon amendments. Soil Biology & Biochemistry, 43(2), 385–392.CrossRefGoogle Scholar
  20. Lam, P., & Kuypers, M. M. (2011). Microbial nitrogen cycling processes in oxygen minimum zones. Annual Review of Marine Science, 3, 317–345.CrossRefGoogle Scholar
  21. Larson, C. (2014). China gets serious about its pollutant-laden soil. Science, 343(6178), 1415–1416.CrossRefGoogle Scholar
  22. Lehmann, J., Rillig, M. C., Thies, J., Masiello, C. A., Hockaday, W. C., & Crowley, D. (2011). Biochar effects on soil biota—a review. Soil Biology & Biochemistry, 43(9), 1812–1836.CrossRefGoogle Scholar
  23. Liu, B., Morkved, P. T., Frostegard, A., & Bakken, L. R. (2010). Denitrification gene pools, transcription and kinetics of NO, N2O and N2 production as affected by soil pH. FEMS Microbiology Ecology, 72(3), 407–417.CrossRefGoogle Scholar
  24. Lozupone, C., Hamady, M., & Knight, R. (2005). UniFrac—an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics, 241(110), 184–186.Google Scholar
  25. Lu, H., Li, Z., Fu, S., Mendez, A., Gasco, G., & Paz-Ferreiro, J. (2015). Combining phytoextraction and biochar addition improves soil biochemical properties in a soil contaminated with Cd. Chemosphere, 119, 209–216.CrossRefGoogle Scholar
  26. Magalhães, C., Costa, J., Teixeira, C., & Bordalo, A. A. (2007). Impact of trace metals on denitrification in estuarine sediments of the Douro River estuary, Portugal. Marine Chemistry, 107(3), 332–341.CrossRefGoogle Scholar
  27. Magalhães, C. M., Machado, A., Matos, P., & Bordalo, A. A. (2011). Impact of copper on the diversity, abundance and transcription of nitrite and nitrous oxide reductase genes in an urban European estuary. FEMS Microbiology Ecology, 77(2), 274–284.CrossRefGoogle Scholar
  28. Martinez-Alonso, M., Escolano, J., Montesinos, E., & Gaju, N. (2010). Diversity of the bacterial community in the surface soil of a pear orchard based on 16S rRNA gene analysis. International Microbiology, 13(3), 123–134.Google Scholar
  29. McKenney, D., & Vriesacker, J. (1985). Effect of cadmium contamination on denitrification processes in Brookston clay and Fox sandy loam. Environmental Pollution Series A, Ecological and Biological, 38(3), 221–233.CrossRefGoogle Scholar
  30. McMillan, A. M. S., Pal, P., Phillips, R. L., Palmada, T., Berben, P. H., Jha, N., Saggar, S., & Luo, J. (2016). Can pH amendments in grazed pastures help reduce N2O emissions from denitrification?—The effects of liming and urine addition on the completion of denitrification in fluvial and volcanic soils. Soil Biology & Biochemistry, 93, 90–104.CrossRefGoogle Scholar
  31. Miller, M. N., Zebarth, B. J., Dandie, C. E., Burton, D. L., Goyer, C., & Trevors, J. T. (2008). Crop residue influence on denitrification, N2O emissions and denitrifier community abundance in soil. Soil Biology & Biochemistry, 40(10), 2553–2562.CrossRefGoogle Scholar
  32. Mora, A. P. D., Ortega-Calvo, J. J., Cabrera, F., & Madejón, E. (2005). Changes in enzyme activities and microbial biomass after “in situ” remediation of a heavy metal-contaminated soil. Applied Soil Ecology, 28(2), 125–137.CrossRefGoogle Scholar
  33. Nelissen, V., Rütting, T., Huygens, D., Staelens, J., Ruysschaert, G., & Boeckx, P. (2012). Maize biochars accelerate short-term soil nitrogen dynamics in a loamy sand soil. Soil Biology & Biochemistry, 55, 20–27.CrossRefGoogle Scholar
  34. Ridnour, L. A., Sim, J. E., Hayward, M. A., Wink, D. A., Martin, S. M., Buettner, G. R., & Spitz, D. R. (2000). A spectrophotometric method for the direct detection and quantitation of nitric oxide, nitrite, and nitrate in cell culture media. Analytical Biochemistry, 281(2), 223–229.CrossRefGoogle Scholar
  35. Sørensen, J. (1978). Denitrification rates in a marine sediment as measured by the acetylene inhibition technique. Applied and Environmental Microbiology, 36(1), 139–143.Google Scholar
  36. Scheer, C., Grace, P. R., Rowlings, D. W., Kimber, S., & Van Zwieten, L. (2011). Effect of biochar amendment on the soil-atmosphere exchange of greenhouse gases from an intensive subtropical pasture in northern New South Wales, Australia. Plant and Soil, 345(1–2), 47–58.CrossRefGoogle Scholar
  37. Schlegel, H. G. (1985). Allgemeine Mikrobiologie. Stuttgart: Georg Thieme Verlag.Google Scholar
  38. Singh, D. K., & Kumar, S. (2008). Nitrate reductase, arginine deaminase, urease and dehydrogenase activities in natural soil (ridges with forest) and in cotton soil after acetamiprid treatments. Chemosphere, 71(3), 412–418.CrossRefGoogle Scholar
  39. Spokas, K. A., & Reicosky, D. C. (2009). Impacts of sixteen different biochars on soil greenhouse gas production. Annals of Environmental Science, 3(1), 4.Google Scholar
  40. Suzuki, S., Kataoka, K., & Yamaguchi, K. (2000). Metal coordination and mechanism of multicopper nitrite reductase. Accounts of Chemical Research, 33(10), 728–735.CrossRefGoogle Scholar
  41. Troy, S. M., Lawlor, P. G., O’ Flynn, C. J., & Healy, M. G. (2013). Impact of biochar addition to soil on greenhouse gas emissions following pig manure application. Soil Biology & Biochemistry, 60, 173–181.CrossRefGoogle Scholar
  42. Uchimiya, M., Wartelle, L. H., Klasson, K. T., Fortier, C. A., & Lima, I. M. (2011). Influence of pyrolysis temperature on biochar property and function as a heavy metal sorbent in soil. Journal of Agricultural and Food Chemistry, 59(6), 2501–2510.CrossRefGoogle Scholar
  43. Urich, T., Lanzén, A., Qi, J., Huson, D. H., Schleper, C., & Schuster, S. C. (2008). Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. PLoS ONE, 3(6), e2527.CrossRefGoogle Scholar
  44. Van Zwieten, L., Singh, B. P., Kimber, S. W. L., Murphy, D. V., Macdonald, L. M., Rust, J., & Morris, S. (2014). An incubation study investigating the mechanisms that impact N2O flux from soil following biochar application. Agriculture, Ecosystems & Environment, 191, 53–62.CrossRefGoogle Scholar
  45. Vasquezmurrieta, M., Cruzmondragon, C., Trujillotapia, N., Herreraarreola, G., Govaerts, B., Vancleemput, O., & Dendooven, L. (2006). Nitrous oxide production of heavy metal contaminated soil. Soil Biology & Biochemistry, 38(5), 931–940.CrossRefGoogle Scholar
  46. Vig, K. (2003). Bioavailability and toxicity of cadmium to microorganisms and their activities in soil: a review. Advances in Environmental Research, 8(1), 121–135.CrossRefGoogle Scholar
  47. Xu, H., Wang, X., Li, H., Yao, H., Su, J., & Zhu, Y. (2014). Biochar impacts soil microbial community composition and nitrogen cycling in an acidic soil planted with rape. Environmental Science & Technology, 48(16), 9391–9399.CrossRefGoogle Scholar
  48. Yang, F., Cao, X., Gao, B., Zhao, L., & Li, F. (2015). Short-term effects of rice straw biochar on sorption, emission, and transformation of soil NH(4)(+)-N. Environmental Science and Pollution Research International, 22, 9184–9192.CrossRefGoogle Scholar
  49. Zhang, H., Voroney, R., & Price, G. (2015). Effects of temperature and processing conditions on biochar chemical properties and their influence on soil C and N transformations. Soil Biology & Biochemistry, 83, 19–28.CrossRefGoogle Scholar
  50. Zumft, W. G. (1997). Cell biology and molecular basis of denitrification. Microbiology and Molecular Biology Reviews, 61, 533–616.Google Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Guanhong Chen
    • 1
  • Zhirong Zhang
    • 1
  • Zhiyuan Zhang
    • 1
  • Renduo Zhang
    • 1
  1. 1.Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology, School of Environmental Science and EngineeringSun Yat-sen UniversityGuangzhouChina

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