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Response of denitrification genes nirS, nirK, and nosZ to irrigation water quality in a Chinese agricultural soil

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Abstract

Purpose

Denitrification is an important biochemical process in global nitrogen cycle, with a potent greenhouse gas product N2O. Wastewater irrigation can result in the changes of soil properties and microbial communities of agricultural soils. The purpose of this study was to examine how the soil denitrification genes responded to different irrigation regimes.

Materials and methods

Soil samples were collected from three rural districts of Beijing (China) with three different irrigation regimes: clean groundwater (CW), reclaimed water (RW), and wastewater (WW). The abundance and diversity of three denitrification microbial genes (nirS, nirK, and nosZ) were examined by real-time polymerase chain reaction (PCR) and denaturing gradient gel electrophoresis (DGGE) molecular approaches.

Results and discussion

The abundance of nirS in the WW treatment was higher than that in the CW treatment, and no significant difference was found between the RW and CW or WW treatments. The abundance of nirK gene of the RW and WW treatments was higher than that of the CW treatment. There was no difference for nosZ gene among the three treatments. Correspondence analysis based on the DGGE profiles showed that there was no obvious difference in the nosZ gene composition, but nirS and nirK genes changed with different irrigation regimes.

Conclusions

Irrigation with unclean water sources enhanced the soil NO −3 content and changed the abundance and composition of soil denitrifiers, and different functional genes had different responses. Irrigation with unclean water sources increased the abundance of nirK gene and changed the community structures of nirS and nirK genes, while nosZ gene was relatively stable in the soil. These results could be helpful to explore the mechanisms of the variation of denitrification processes under long-term wastewater irrigation and partially explain the reason of more N2O output in the field with wastewater irrigation.

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References

  • Barton L, McLay CDA, Schipper LA, Smith CT (1999) Denitrification rates in a wastewater-irrigated forest soil in New Zealand. J Environ Qual 28(6):2008–2014

    Article  CAS  Google Scholar 

  • Barton L, Schipper LA, Smith CT, McLay CDA (2000) Denitrification enzyme activity is limited by soil aeration in a wastewater irrigated forest soil. Biol Fertil Soils 32(5):385–389

    Article  CAS  Google Scholar 

  • Bouwman AF (1990) Exchange of greenhouse gases between terrestrial ecosystems and the atmosphere. In: Bouwman AF (ed) Soils and the greenhouse effect. Wiley, Chichester, pp 100–120

    Google Scholar 

  • Braker G, Tiedje JM (2003) Nitric oxide reductase (norB) genes from pure cultures and environmental samples. Appl Environ Microbiol 69(6):3476–3483

    Article  CAS  Google Scholar 

  • Chronakova A, Radl V, Cuhel J, Simek M, Elhottova D, Engel M, Schloter M (2009) Overwintering management on upland pasture causes shifts in an abundance of denitrifying microbial communities, their activity and N2O-reducing ability. Soil Biol Biochem 41(6):1132–1138

    Article  CAS  Google Scholar 

  • Cong XH, Zhao YF (2009) Recycle and usage of reclaimed water in Beijing City. Beijing Water Utilities 1:10–12

    Google Scholar 

  • Dandie CE, Burton DL, Zebarth BJ, Henderson SL, Trevors JT, Goyer C (2008) Changes in bacterial denitrifier community abundance over time in an agricultural field and their relationship with denitrification activity. Appl Environ Microbiol 74(19):5997–6005

    Article  CAS  Google Scholar 

  • Djigal D, Baudoin E, Plilippot L, Brauman A, Villenave C (2010) Shifts in size, genetic structure and activity of the soil denitrifier community by nematode grazing. Eur J Soil Biol 46(2):112–118

    Article  CAS  Google Scholar 

  • Enwall K, Philippot L, Hallin S (2005) Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Appl Environ Microbiol 71(12):8335–8343

    Article  CAS  Google Scholar 

  • Franklin RB, Mills AL (2003) Multi-scale variation in spatial heterogeneity for microbial community structure in an eastern Virginia agricultural field. FEMS Microbiol Ecol 44(3):335–346

    Article  CAS  Google Scholar 

  • Friedel JK, Langer T, Siebe C, Stahr K (2000) Effects of long-term waste water irrigation on soil organic matter, soil microbial biomass and its activities in central Mexico. Biol Fertil Soils 31(5):414–421

    Article  Google Scholar 

  • Hai B, Diallo NH, Sall S, Haesler F, Schauss K, Bonzi M, Assigbetse K, Chotte JL, Munch JC, Schloter M (2009) Quantification of key genes steering the microbial nitrogen cycle in the rhizosphere of sorghum cultivars in tropical agroecosystems. Appl Environ Microbiol 75(15):4993–5000

    Article  CAS  Google Scholar 

  • Hallin S, Lindgren PE (1999) PCR detection of genes encoding nitrile reductase in denitrifying bacteria. Appl Environ Microbiol 65(4):1652–1657

    CAS  Google Scholar 

  • Hallin S, Jones CM, Schloter M, Philippot L (2009) Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J 3(5):597–605

    Article  CAS  Google Scholar 

  • He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di HJ (2007) Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol 9(9):2364–2374

    Article  CAS  Google Scholar 

  • Henry S, Bru D, Stres B, Hallet S, Philippot L (2006) Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl Environ Microbiol 72(8):5181–5189

    Article  CAS  Google Scholar 

  • Intergovernmental Panel on Climate Change (IPCC) (2007) Climate Change 2007: The Physical Science Basis. Working Group I Contribution to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Solomon et al. (eds). Cambridge University Press, Cambridge

  • Kandeler E, Deiglmayr K, Tscherko D, Bru D, Philippot L (2006) Abundance of narG, nirS, nirK, and nosZ genes of denitrifying bacteria during primary successions of a glacier foreland. Appl Environ Microbiol 72(9):5957–5962

    Article  CAS  Google Scholar 

  • Kloos K, Mergel A, Rosch C, Bothe H (2001) Denitrification within the genus Azospirillum and other associative bacteria. Aust J Plant Physiol 28(9):991–998

    Google Scholar 

  • Ladd JN, Foster RC, Skjemstad JO (1993) Soil structure-carbon and nitrogen-metabolism. Geoderma 56(1–4):401–434

    Article  CAS  Google Scholar 

  • Mapanda F, Mangwayana EN, Nyamangara J, Giller KE (2005) The effect of long-term irrigation using wastewater on heavy metal contents of soils under vegetables in Harare, Zimbabwe. Agric Ecosyst Environ 107(2–3):151–165

    Article  CAS  Google Scholar 

  • Michotey V, Mejean V, Bonin P (2000) Comparison of methods for quantification of cytochrome cd(1)-denitrifying bacteria in environmental marine samples. Appl Environ Microbiol 66(4):1564–1571

    Article  CAS  Google Scholar 

  • Philippot L, Hojberg O (1999) Dissimilatory nitrate reductases in bacteria. Biochim Et Biophys Acta Gene Struct Expr 1446(1–2):1–23

    Article  CAS  Google Scholar 

  • Qian YL, Mecham B (2005) Long-term effects of recycled wastewater irrigation on soil chemical properties on golf course fairways. Agron J 97(3):717–721

    Article  CAS  Google Scholar 

  • Smith CJ, Nedwell DB, Dong LF, Osborn AM (2007) Diversity and abundance of nitrate reductase genes (narG and napA), nitrite reductase genes (nirS and nrfA), and their transcripts in estuarine sediments. Appl Environ Microbiol 73(11):3612–3622

    Article  CAS  Google Scholar 

  • Throback IN, Enwall K, Jarvis A, Hallin S (2004) Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiol Ecol 49(3):401–417

    Article  CAS  Google Scholar 

  • Wallenstein MD (2004) Effects of increased nitrogen deposition on forest soil nitrogen cycling and microbial community structure. Duke University, Durham

    Google Scholar 

  • Wolsing M, Prieme A (2004) Observation of high seasonal variation in community structure of denitrifying bacteria in arable soil receiving artificial fertilizer and cattle manure by determining T-RFLP of nir gene fragments. FEMS Microbiol Ecol 48(2):261–271

    Article  CAS  Google Scholar 

  • Yang J, Zheng YM, Chen TB, Huang ZC, Luo JF, Liu HL, Wu WY, Chen YC (2005) Accumulation and temporal variation of heavy metals in the soils from the Liangfeng Irrigated Area of Tongzhou, Beijing City. Acta Scientiae Circumstantiae 25(9):1175–1181

    CAS  Google Scholar 

  • Yoshida M, Ishii S, Otsuka S, Senoo K (2009) Temporal shifts in diversity and quantity of nirS and nirK in a rice paddy field soil. Soil Biol Biochem 41(10):2044–2051

    Article  CAS  Google Scholar 

  • Yoshida M, Ishii S, Otsuka S, Senoo K (2010) nirK-harboring denitrifiers are more responsive to denitrification-inducing conditions in rice paddy soil than nirS-harboring bacteria. Microbes Environ 25(1):45–48

    Article  Google Scholar 

  • Zheng YM, Chen TB, He JZ (2008) Multivariate geostatistical analysis of heavy metals in topsoils from Beijing, China. J Soils Sediments 8(1):51–58

    Article  CAS  Google Scholar 

  • Zou J, Liu S, Qin Y, Pan G, Zhu D (2009) Sewage irrigation increased methane and nitrous oxide emissions from rice paddies in southeast China. Agric Ecosyst Environ 129(4):516–522

    Article  CAS  Google Scholar 

  • Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61(4):592

    Google Scholar 

Download references

Acknowledgments

This work was supported by the Ministry of Sciences and Technology (2009AA06Z402), the Chinese Academy of Sciences (KZCX1-YW-06-03, KSCX2-YW-G072) and the Natural Science Foundation of China (41090281, 41025004, 50921064).

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Authors and Affiliations

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

    Zhi-Feng Zhou, Yuan-Ming Zheng, Ju-Pei Shen, Li-Mei Zhang & Ji-Zheng He

  2. Graduate University, Chinese Academy of Sciences, Beijing, 100049, China

    Zhi-Feng Zhou

  3. College of Resources and Environment, Southwest University, Chongqing, 400716, China

    Zhi-Feng Zhou

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  1. Zhi-Feng Zhou
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  2. Yuan-Ming Zheng
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  3. Ju-Pei Shen
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  4. Li-Mei Zhang
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  5. Ji-Zheng He
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Correspondence to Ji-Zheng He.

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Responsible editor: Zhihong Xu

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Zhou, ZF., Zheng, YM., Shen, JP. et al. Response of denitrification genes nirS, nirK, and nosZ to irrigation water quality in a Chinese agricultural soil. Environ Sci Pollut Res 18, 1644–1652 (2011). https://doi.org/10.1007/s11356-011-0482-8

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  • DOI: https://doi.org/10.1007/s11356-011-0482-8

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