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Increased copper levels inhibit denitrification in urban soils

Published online by Cambridge University Press:  06 December 2018

Shun LI ,
Xiaoru YANG ,
Daniel BUCHNER ,
Haitao WANG ,
Huijuan XU ,
Stefan B. HADERLEIN  and
Yongguan ZHU
Shun LI
Affiliation:
Key Lab of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, 1799 Jimei Road, Xiamen 361021, China. Email: xryang@iue.ac.cn Center for Excellence in Regional Atmospheric Environment, Institute of Urban Environment, Chinese Academy of Sciences, 1799 Jimei Road, Xiamen 361021, China. Center for Applied Geosciences, University of Tübingen, Hölderlinstr. 12, Tübingen 72074, Germany.
Xiaoru YANG*
Affiliation:
Key Lab of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, 1799 Jimei Road, Xiamen 361021, China. Email: xryang@iue.ac.cn Center for Excellence in Regional Atmospheric Environment, Institute of Urban Environment, Chinese Academy of Sciences, 1799 Jimei Road, Xiamen 361021, China.
Daniel BUCHNER
Affiliation:
Center for Applied Geosciences, University of Tübingen, Hölderlinstr. 12, Tübingen 72074, Germany.
Haitao WANG
Affiliation:
Key Lab of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, 1799 Jimei Road, Xiamen 361021, China. Email: xryang@iue.ac.cn
Huijuan XU
Affiliation:
Key Lab of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, 1799 Jimei Road, Xiamen 361021, China. Email: xryang@iue.ac.cn College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China.
Stefan B. HADERLEIN
Affiliation:
Center for Applied Geosciences, University of Tübingen, Hölderlinstr. 12, Tübingen 72074, Germany.
Yongguan ZHU
Affiliation:
Key Lab of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, 1799 Jimei Road, Xiamen 361021, China. Email: xryang@iue.ac.cn Center for Excellence in Regional Atmospheric Environment, Institute of Urban Environment, Chinese Academy of Sciences, 1799 Jimei Road, Xiamen 361021, China.
*
*Corresponding author
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Abstract

The consequences of urbanisation for Earth's biogeochemical cycles are largely unexplored. Copper (Cu) in urban soils is being accumulated mainly due to anthropogenic activities under rapid urbanisation. The increasing Cu concentrations may contribute to altering soil nitrogen (N) cycling in urban ecosystems through modulating denitrification processes. This research aims to identify how Cu impacts urban soil denitrification functions and denitrifier abundance. An urban park soil with a background total Cu concentration of 7.9μgg–1 was incubated anaerobically with different Cu amendments (10, 20, 40, 80 and 160μg Cu g–1 soil), similar to prevalent Cu contents in urban soils. We evaluated the soil denitrification functions using the acetylene (C2H2) inhibition method and assessed the denitrifier abundance by quantitative polymerase chain reaction (qPCR) analyses of denitrifying marker genes (nirK, nirS and nosZ). At the function level, we observed that both the potential soil denitrification activity and the N2O emission rate due to denitrification were significantly (P<0.05) inhibited by Cu; even the lowest Cu addition (10μg Cu g–1 soil) drastically affected the denitrification function. Moreover, Cu significantly (P<0.05) decreased the abundance of nirK and nirS genes at the additions of 160μg Cu g–1 soil and 40μg Cu g–1 soil, respectively, whereas it had no clear impact on nosZ gene copies. Further correlation analyses revealed that the potential denitrification activity was positively correlated to the copy numbers of nirK and nirS genes, but it was not correlated to nosZ gene abundance. These findings indicate that Cu additions inhibited soil denitrification function and decreased denitrifier abundance in the investigated urban park soil. Our results suggest that Cu accumulation in urban soils, resulting from urbanisation, may generally influence denitrification in urban ecosystems.

Keywords

N2OnirKnirSnosZurbanisation
Type
Articles
Information
Earth and Environmental Science Transactions of The Royal Society of Edinburgh , Volume 109 , Issue 3-4: Earth Surface Processes and Environmental Sustainability in China , September 2018 , pp. 421 - 427
Copyright
Copyright © The Royal Society of Edinburgh 2018 

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References

6. References

Aoyama, M. & Nagumo, T. 1996. Factors affecting microbial biomass and dehydrogenasc activity in apple orchard soils with heavy metal accumulation. Soil Science and Plant Nutrition 42, 821–831.Google Scholar
Bardgett, R. D., Speir, T. W., Ross, D. J., Yeates, G. W. & Kettles, H. A. 1994. Impact of pasture contamination by copper, chromium, and arsenic timber preservative on soil microbial properties and nematodes. Biology and Fertility of Soils 18, 71–79.Google Scholar
Black, A., Hsu, P. C. L., Hamonts, K. E., Clough, T. J. & Condron, L. M. 2016. Influence of copper on expression of nirS, norB and nosZ and the transcription and activity of NIR, NOR and N2OR in the denitrifying soil bacteria Pseudomonas stutzeri. Microbial Biotechnology 9, 381–388.Google Scholar
Brown, D. G., Johnson, K. M., Loveland, T. R. & Theobald, D. M. 2005. Rural land-use trends in the conterminous United States, 1950–2000. Ecological Applications 15, 1851–1863.Google Scholar
Bru, D., Ramette, A., Saby, N. P. A., Dequiedt, S., Ranjard, L., Jolivet, C., Arrouays, D. & Philippot, L. 2011. Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale. The ISME Journal 5, 532–542.Google Scholar
Cheng, H., Li, M., Zhao, C., Li, K., Peng, M., Qin, A. & Cheng, X. 2014. Overview of trace metals in the urban soil of 31 metropolises in China. Journal of Geochemical Exploration 139, 31–52.Google Scholar
China Environmental Monitoring Station. 1990. Background values of elements in soils of China. Beijing: China Environmental Press. 501 pp. [In Chinese.]Google Scholar
Fang, Y., Koba, K., Makabe, A., Zhu, F., Fan, S., Liu, X. & Yoh, M. 2012. Low δ18O values of nitrate produced from nitrification in temperate forest soils. Environmental Science & Technology 46, 8723–8730.Google Scholar
Felgate, H., Giannopoulos, G., Sullivan, M. J., Gates, A. J., Clarke, T. A., Baggs, E., Rowley, G. & Richardson, D. J. 2012. The impact of copper, nitrate and carbon status on the emission of nitrous oxide by two species of bacteria with biochemically distinct denitrification pathways. Environmental Microbiology 14, 1788–1800.Google Scholar
Giller, K. E., Witter, E. & Mcgrath, S. P. 1998. Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biology and Biochemistry 30, 1389–1414.Google Scholar
Granger, J. & Ward, B. B. 2003. Accumulation of nitrogen oxides in copper-limited cultures of denitrifying bacteria. Limnology and Oceanography 48, 313–318.Google Scholar
Guo, G. X., Deng, H., Qiao, M., Yao, H. Y. & Zhu, Y. G. 2013. Effect of long-term wastewater irrigation on potential denitrification and denitrifying communities in soils at the watershed scale. Environmental Science & Technology 47, 3105–3113.Google Scholar
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.Google Scholar
Hallin, S. & Lindgren, P. E. 1999. PCR detection of genes encoding nitrite reductase in denitrifying bacteria. Applied and Environmental Microbiology 65, 1652–1657.Google Scholar
Holtan-Hartwig, L., Bechmann, M., Høyås, T. R., Linjordet, R. & Bakken, L. R. 2002. Heavy metals tolerance of soil denitrifying communities: N2O dynamics. Soil Biology and Biochemistry 34, 1181–1190.Google Scholar
Kaye, J. P., Groffman, P. M., Grimm, N. B., Baker, L. A. & Pouyat, R. V. 2006. A distinct urban biogeochemistry? Trends in Ecology & Evolution 21, 192–199.Google Scholar
Lee, C. S. L., Li, X., Shi, W., Cheung, S. C. N. & Thornton, I. 2006. Metal contamination in urban, suburban, and country park soils of Hong Kong: a study based on GIS and multivariate statistics. Science of the Total Environment 356, 45–61.Google Scholar
Lehmann, A. & Stahr, K. 2007. Nature and significance of anthropogenic urban soils. Journal of Soils and Sediments 7, 247–260.Google Scholar
Li, S., Deng, H., Rensing, C. & Zhu, Y. G. 2014. Compaction stimulates denitrification in an urban park soil using 15N tracing technique. Environmental Science and Pollution Research 21, 3783–3791.Google Scholar
Li, X. F., Sun, J. W., Huang, Y. Z., Ma, Y. B. & Zhu, Y. G. 2010. Copper toxicity thresholds in Chinese soils based on substrate-induced nitrification assay. Environmental Toxicology and Chemistry 29, 294–300.Google Scholar
Luo, X. S., Yu, S., Zhu, Y. G. & Li, X. D. 2012. Trace metal contamination in urban soils of China. Science of the Total Environment , 17–30.Google Scholar
Luo, X. S., Xue, Y., Wang, Y. L., Cang, L., Xu, B. & Ding, J. 2015. Source identification and apportionment of heavy metals in urban soil profiles. Chemosphere 127, 152–157.Google Scholar
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, 332–341.Google Scholar
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, 274–284.Google Scholar
Matsubara, T., Frunzke, K. & Zumft, W. G. 1982. Modulation by copper of the products of nitrite respiration in Pseudomonas perfectomarinus. Journal of Bacteriology 149, 816–823.Google Scholar
Moffett, J. W., Tuit, C. B. & Ward, B. B. 2012. Chelator-induced inhibition of copper metalloenzymes in denitrifying bacteria. Limnology and Oceanography 57, 272.Google Scholar
Molstad, L., Dörsch, P. & Bakken, L. R. 2007. Robotized incubation system for monitoring gases (O2, NO, N2O, N2) in denitrifying cultures. Journal of Microbiological Methods 71, 202–211.Google Scholar
Muyzer, G., De Waal, E. C. & Uitterlinden, A. G. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Applied and Environmental Microbiology 59, 695–700.Google Scholar
Myrold, D. D. & Tiedje, J. M. 1985. Establishment of denitrification capacity in soil: effects of carbon, nitrate and moisture. Soil Biology and Biochemistry 17, 819–822.Google Scholar
Petersen, D. G., Blazewicz, S. J., Firestone, M., Herman, D. J., 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. Environmental Microbiology 14, 993–1008.Google Scholar
Pickett, S. T., Cadenasso, M. L., Grove, J. M., Boone, C. G., Groffman, P. M., Irwin, E., Kaushal, S. S., Marshall, V., McGrath, B. P., Nilon, C. H., Pouyat, R. V., Szlavecz, K., Troy, A. & Warren, P. 2011. Urban ecological systems: scientific foundations and a decade of progress. Journal of Environmental Management 92, 331–362.Google Scholar
Ravishankara, A. R., Daniel, J. S. & Portmann, R. W. 2009. Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326, 123–125.Google Scholar
Rooney, C. P., Zhao, F. J. & McGrath, S. P. 2006. Soil factors controlling the expression of copper toxicity to plants in a wide range of European soils. Environmental Toxicology and Chemistry 25, 726–732.Google Scholar
Sakadevan, K., Zheng, H. & Bavor, H. J. 1999. Impact of heavy metals on denitrification in surface wetland sediments receiving wastewater. Water Science and Technology 40, 349–355.Google Scholar
State Environmental Protection Administration of China. 2008. Environmental Quality Standards for Soils (GB 15618–2008). Beijing: State Environmental Protection Administration of China. [In Chinese.]Google Scholar
Sullivan, M. J., Gates, A. J., Appia-Ayme, C., Rowley, G. & Richardson, D. J. 2013. Copper control of bacterial nitrous oxide emission and its impact on vitamin B12-dependent metabolism. Proceedings of the National Academy of Sciences 110, 19926–31.Google Scholar
Throbäck, I. N., Enwall, K., Jarvis, Å. & Hallin, S. 2004. Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiology Ecology 49, 401–417.Google Scholar
Vega, F. A., Andrade, M. L. & Covelo, E. F. 2010. Influence of soil properties on the sorption and retention of cadmium, copper and lead, separately and together, by 20 soil horizons: comparison of linear regression and tree regression analyses. Journal of Hazardous Materials 174, 522–533.Google Scholar
Wang, Q., Burger, M., Doane, T. A., Horwath, W. R., Castillo, A. R. & Mitloehner, F. M. 2013. Effects of inorganic v. organic copper on denitrification in agricultural soil. Advances in Animal Biosciences 4(s1), 42–49.Google Scholar
Wei, B. & Yang, L. 2010. A review of heavy metal contaminations in urban soils, urban road dusts and agricultural soils from China. Microchemical Journal 94, 99–107.Google Scholar
Xu, D., Zhou, P., Zhan, J., Gao, Y., Dou, C. & Sun, Q. 2013. Assessment of trace metal bioavailability in garden soils and health risks via consumption of vegetables in the vicinity of Tongling mining area, China. Ecotoxicology and Environmental Safety 90, 103–111.Google Scholar
Zhu, W. X. & Carreiro, M. M. 2004. Temporal and spatial variations in nitrogen transformations in deciduous forest ecosystems along an urban-rural gradient. Soil Biology and Biochemistry 36, 267–278.Google Scholar
Zhu, Y. G., Ioannidis, J. P., Li, H., Jones, K. C. & Martin, F. L. 2011. Understanding and harnessing the health effects of rapid urbanization in China. Environmental Science & Technology 45, 5099–5104.Google Scholar
Zumft, W. G. 1997. Cell biology and molecular basis of denitrification. Microbiology and Molecular Biology Reviews 61, 533–616.Google Scholar