Skip to main content
SpringerLink
Log in

Elevated N2O emission by the rice roots: based on the abundances of narG and bacterial amoA genes

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Rice fields are an important source of nitrous oxide (N2O), where rice plants could act as a key factor controlling N2O fluxes during the flooding-drying process; however, the microbial driving mechanisms are unclear. In this study, specially designed equipment was used to grow rice plants and collect emitted N2O from the root-growing zone (zone A), root-free zones (zones B, C, and D) independently, at tillering and booting stages under flooding and drying conditions. Soil samples from the four zones were also taken separately. Nitrifying and denitrifying community abundances were detected using quantitative polymerase chain reaction (qPCR). The N2O emission increased significantly along with drying, but the N2O emission capabilities varied among the four zones under drying, while zone B possessed the highest N2O fluxes that were 2.7~4.5 times higher than those from zones C and D. However, zone A showed N2O consumption potential. Notably, zone B also harbored the highest numbers of narG-containing denitrifiers and amoA-containing nitrifiers under drying at both tillering and booting stages. This study demonstrates that drying caused significant increase in N2O emission from rhizosphere soil, in which the higher abundance of AOB would help to produce more nitrate and significantly higher narG-containing microbes would drive more N2O production and emission.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Akiyama H, Yagi K, Yan X (2005) Direct N2O emissions from rice paddy fields: summary of available data. Glob Biogeochem Cycles. doi:10.1029/2004GB002378

    Google Scholar 

  • Arth I, Frenzel P (2000) Nitrification and denitrification in the rhizosphere of rice: the detection of processes by a new multi-channel electrode. Biol Fertil Soils 31:427–435

    Article  CAS  Google Scholar 

  • Bateman EJ, Baggs EM (2005) Contributions of nitrification and denitrification to N2O emissions from soils at different water-filled pore space. Biol Fertil Soils 41:379–388

    Article  CAS  Google Scholar 

  • Baudoin E, Benizri E, Guckert A (2003) Impact of artificial root exudates on the bacterial community structure in bulk soil and maize rhizosphere. Soil Biol Biochem 35:1183–1192

    Article  CAS  Google Scholar 

  • Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83

    Article  CAS  Google Scholar 

  • Bouwman AF, Boumans LJM, Batjes NH (2002) Emissions of N2O and NO from fertilized fields: summary of available measurement data. Glob Biogeochem Cycles. doi:10.1029/2001GB001811

    Google Scholar 

  • Bowatte S, Jia ZJ, Ishihara R, Nakajima Y, Asakawa S, Kimura M (2006) Molecular analysis of the ammonia-oxidizing bacterial community in the surface soil layer of Japanese paddy field. Soil Sci Plant Nutr 52:427–431

    Article  CAS  Google Scholar 

  • Bowatte S, Asakawa S, Okada M, Kobayashi K, Kimura M (2007) Effect of elevated atmospheric CO2 concentration on ammonia oxidizing bacteria communities inhabiting in rice roots. Soil Sci Plant Nutr 53:32–39

    Article  CAS  Google Scholar 

  • Boyd ES, Lange RK, Mitchell AC (2011) Diversity, abundance, and potential activity of nitrifying and nitrate-reducing microbial assemblages in a subglacial ecosystem. Appl Environ Microbiol 77:4778–4787

    Article  CAS  Google Scholar 

  • Braker G, Conrad R (2011) Diversity, structure, and size of N2O-producing microbial communities in soils-what matters for their functioning? Adv Appl Microbiol 75:34–57

    Google Scholar 

  • Briones AM, Okabe S, Umemiya Y, Ramsing NB, Reichardt W, Okuyama H (2002) Influence of different cultivars on populations of ammonia-oxidizing bacteria in the root environment of rice. Appl Environ Microbiol 68:3067–3075

    Article  CAS  Google Scholar 

  • Cai ZC, Xing GX, Yan XY, Xu H, Tsuruta H, Yagi K, Minami K (1997) Methane and nitrous oxide emissions from rice paddy fields as affected by nitrogen fertilizers and water management. Plant Soil 196:7–14

    Article  CAS  Google Scholar 

  • Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. The ISME J 8:790–803

    Article  CAS  Google Scholar 

  • Chen Z, Luo XQ, Hu RG, Wu MN, Wu JS (2010) Impact of long-term fertilization on the composition of denitrifier communities based on nitrite reductase analyses in a paddy soil. Microb Ecol 60:850–861

    Article  CAS  Google Scholar 

  • Chen Z, Liu JB, Wu MN, Xie XL, Wu JS, Wei WX (2012) Differentiated response of denitrifying communities to fertilization regime in paddy soil. Microb Ecol 63:446–459

    Article  Google Scholar 

  • Chu HY, Morimoto S, Fujii T, Yagi K, Nishimura S (2009) Soil ammonia-oxidizing bacterial communities in paddy rice fields as affected by upland conversion history. Soil Sci Soc Am J 73:2026–2031

    Article  CAS  Google Scholar 

  • Chu HY, Morimoto S, Fujii T, Yagi K, Nishimura S (2010) Soil ammonia-oxidizing bacterial communities in paddy rice fields as affected by upland conversion history. Soil Sci Soc Am J 73:2026–2031

    Article  Google Scholar 

  • Conrad R, Seiler W, Bunse G (1983) Factors influencing the loss of fertilizer nitrogen into the atmosphere as N2O. J Geophys Res [Oceans] 88:6709–6718

    Article  CAS  Google Scholar 

  • Delaune RD, Lindau CW, Sulaeman E, Jugsujinda A (1998) Nitrification and denitrification estimates in a Louisiana swamp forest soil as assessed by 15N isotope dilution and direct gaseous measurements. Water Air Soil Pollut 106:149–161

    Article  CAS  Google Scholar 

  • Devêvre OC, Horwáth WR (2000) Decomposition of rice straw and microbial carbon use efficiency under different soil temperatures and moistures. Soil Biol Biochem 32:1773–1785

    Article  Google Scholar 

  • Di HJ, Cameron KC, Shen JP, Winefield CS, Callaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621–624

    Article  CAS  Google Scholar 

  • Frolking S, Qiu JJ, Boles S, Xiao XM, Liu JY, Zhuang YH, Li CS, Qin XG (2002) Combining remote sensing and ground census data to develop new maps of the distribution of rice agriculture in China. Glob Biogeochem Cycles. doi:10.1029/2001GB001425

    Google Scholar 

  • Glab T, Gondek K (2013) The influence of soil compaction on chemical properties of mollic fluvisol soil under Lucerne (Medicago sativa l.). Pol J Environ Stud 22:107–113

    Google Scholar 

  • Hamonts K, Clough TJ, Stewart A, Clinton PW, Richardson AE, Wakelin SA (2013) Effect of nitrogen and waterlogging on denitrifier gene abundance, community structure and activity in the rhizosphere of wheat. FEMS Microbiol Ecol 83:568–584

    Article  CAS  Google Scholar 

  • Henderson SL, Dandie CE, Patten CL, Zebarth BJ, Burton DL, Trevors JT, Goyer C (2010) Changes in denitrifier abundance, denitrification gene mRNA levels, nitrous oxide emissions, and denitrification in anoxic soil microcosms amended with glucose and plant residues. Appl Environ Microbiol 76:2155–2164

    Article  CAS  Google Scholar 

  • Henry S, Baudoin E, Lopez-Gutierrez JC, Martin-Laurent F, Baumann A, Philippot L (2004) Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. J Microbiol Methods 59:327–335

    Article  CAS  Google Scholar 

  • Hou AX, Chen GX, Wang ZP, Cleemput OV, Patrick WH (2000) Methane and nitrous oxide emissions from a rice field in relation to soil redox and microbiological processes. Soil Sci Soc Am J 64:2180–2186

    Article  CAS  Google Scholar 

  • Isermann K (1994) Agriculture’s share in the emission of trace gases affecting the climate and some cause-oriented proposals for sufficiently reducing this share. Environ Pollut 83:95–111

    Article  CAS  Google Scholar 

  • Ishii S, Ikeda S, Minamisawa K, Senoo K (2011) Nitrogen cycling in rice paddy environments: past achievements and future challenges. Microbes Environ 26:282–292

    Article  Google Scholar 

  • Jackson LE, Burger M, Cavagnaro TR (2008) Roots, nitrogen transformations, and ecosystem services. Annu Rev Plant Biol 59:341–363

    Article  CAS  Google Scholar 

  • Jensen K, Revsbech NP, Nielsen LP (1993) Microscale distribution of nitrification activity in sediment determined with a shielded microsensor for nitrate. Appl Environ Microbiol 59:3287–3296

    CAS  Google Scholar 

  • Jia ZJ, Conrad R (2009) Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671

    Article  CAS  Google Scholar 

  • Jiao ZH, Hou AX, Shi Y, Huang GH, Wang YH, Chen X (2006) Water management influencing methane and nitrous oxide emissions from rice field in relation to soil redox and microbial community. Commun Soil Sci Plant Anal 37:1889–1903

    Article  CAS  Google Scholar 

  • Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205:25–44

    Article  CAS  Google Scholar 

  • Jørgensen CJ, Struwe S, Elberling B (2012) Temporal trends in N2O flux dynamics in a Danish wetland-effects of plant-mediated gas transport of N2O and O2 following changes in water level and soil mineral-N availability. Glob Chang Biol 18:210–222

    Article  Google Scholar 

  • Keeney DR, Sahrawat KL (1986) Nitrogen transformations in flooded rice soils. Fert Res 9:15–38

    Article  CAS  Google Scholar 

  • Kirk GJD (2001) Plant-mediated processes to acquire nutrients: nitrogen uptake by rice plants. Plant Soil 232:129–134

    Article  CAS  Google Scholar 

  • Kirk GJD, Begg CBM, Solivas JL (1993) The chemistry of the lowland rice rhizosphere. Plant Soil 155:83–86

    Article  Google Scholar 

  • Kleineidam K, Košmrlj K, Kublik S, Palmer I, Pfab H, Ruser R, Schloter M (2011) Influence of the nitrification inhibitor 3, 4-dimethylpyrazole phosphate (DMPP) on ammonia-oxidizing bacteria and archaea in rhizosphere and bulk soil. Chemosphere 84:182–186

    Article  CAS  Google Scholar 

  • Kögel-Knabner I, Amelung W, Cao ZH, Fiedler S, Frenzel P, Jahn R, Kalbitz K, Kölbl A, Schloter M (2010) Biogeochemistry of paddy soils. Geoderma 157:1–14

    Article  Google Scholar 

  • Kraffczyk I, Trolldenier G, Beringer H (1984) Soluble root exudates of maize: influence of potassium supply and rhizosphere microorganisms. Soil Biol Biochem 16:315–322

    Article  CAS  Google Scholar 

  • Li ZG, Yu S, Pan YH, Wang JH, Wu SC (1999) Spatial variability of ecological factor controlling nitrification-denitrification in rice rhizosphere. Acta Pedol Sin 36:111–117 (in Chinese)

    Google Scholar 

  • Li CS, Frolking S, Xiao XM, Moore B, Boles S, Qiu JJ, Huang Y, Salas W, Sass R (2005) Modeling impacts of farming management alternatives on CO2, CH4, and N2O emissions: a case study for water management of rice agriculture of China. Glob Biogeochem Cycles. doi:10.1029/2004GB002341

    Google Scholar 

  • Li YL, Fan XR, Shen QR (2008) The relationship between rhizosphere nitrification and nitrogen-use efficiency in rice plants. Plant Cell Environ 31:73–85

    Google Scholar 

  • Liu SW, Qin YM, Zou JW, Liu QH (2010) Effects of water regime during rice-growing season on annual direct N2O emissions in a paddy rice-winter wheat rotation system in southeast China. Sci Total Environ 408:906–913

    Article  CAS  Google Scholar 

  • Liu JB, Hou HJ, Sheng R, Chen Z, Zhu YJ, Qin HL, Wei WX (2012) Denitrifying communities differentially respond to flooding drying cycles in paddy soils. Appl Soil Ecol 62:155–162

    Article  Google Scholar 

  • Liu BB, Frostegård Å, Bakken LR (2014) Impaired reduction of N2O to N2 in acid soils is due to a posttranscriptional interference with the expression of nosZ. MmBio 5:e01383–e01314. doi:10.1128/mBio.01383-14

    Google Scholar 

  • Minami K (1987) Emission of nitrous oxide (N2O) from agro-ecosystem. Japan Agricultural Research Quarterly 21:21–27

    Google Scholar 

  • Mosier AR, Duxbury JM, Freney JR, Heinemeyer O, Minami K (1998) Assessing and mitigating N2O emissions from agricultural soils. Clim Chang 40:7–38

    Article  CAS  Google Scholar 

  • Nicolaisen MH, Risgaard-Petersen N, Revsbech NP, Reichardt W, Ramsing NB (2004) Nitrification-denitrification dynamics and community structure of ammonia oxidizing bacteria in a high yield irrigated Philippine rice field. FEMS Microbiol Ecol 49:359–369

    Article  CAS  Google Scholar 

  • Nie SA, Xu HJ, Li S, Li H, Su JQ (2014) Relationships between abundance of microbial functional genes and the status and fluxes of carbon and nitrogen in rice rhizosphere and bulk soils. Pedosphere 24:645–651

    Article  Google Scholar 

  • Nie SA, Li H, Yang XR, Zhang ZJ, Wen BS, Huang FY, Zhu GB, Zhu YG (2015) Nitrogen loss by anaerobic oxidation of ammonium in rice rhizosphere. The ISME J. doi:10.1038/ismej.2015.25

    Google Scholar 

  • Palmer K, Drake HL, Horn MA (2010) Association of novel and highly diverse acid-tolerant denitrifiers with N2O fluxes of an acidic fen. Applied & Environmental Microbiology 76:1125–1134

    Article  CAS  Google Scholar 

  • Philippot L, Raaijmakers JM, emanceau PL, Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799

  • Rao PSC, Jessup RE, Reddy KR (1984) Simulation of nitrogen dynamics in flooded soils. Soil Sci 138:54–62

    Article  CAS  Google Scholar 

  • Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125

    Article  CAS  Google Scholar 

  • Reddy KR (1982) Nitrogen cycling in a flooded-soil ecosystem planted to rice (Oryza sativa L.). Plant Soil 67:209–220

    Article  CAS  Google Scholar 

  • Romain B, Leadley PW, Hungate BA (2005) Global change, nitrification, and denitrification: a review. Glob Biogeochem Cycles 19:341–356

    Google Scholar 

  • Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712

    CAS  Google Scholar 

  • Rovira AD (1965) Plant root exudates and their influence upon soil microorganisms. Ecology of Soil-borne Plant Pathogens 1:170–186

    Google Scholar 

  • Ruser R, Flessa H, Russow R, Schmidt G, Buegger F, Munch JC (2006) Emission of N2O, N2 and CO2 from soil fertilized with nitrate: effect of compaction, soil moisture and rewetting. Soil Biol Biochem 38:263–274

    Article  CAS  Google Scholar 

  • Savant NK, DeDatta SK (1982) Nitrogen transformations in wetland rice soils. Adv Agron 35:241–302

    Article  CAS  Google Scholar 

  • Skiba U, Fowler D, Smith KA (1997) Nitric oxide emissions from agricultural soils in temperate and tropical climates: sources, controls and mitigation options. Nutr Cycl Agroecosyst 48:139–153

    Article  CAS  Google Scholar 

  • Smith MS, Tiedje JM (1979) The effect of roots on soil denitrification. Soil Sci Soc Am J 43:951–955

    Article  CAS  Google Scholar 

  • Stepniewski W, Gliński J, Ball BC (1994) Effects of compaction on soil aeration properties. Dev Agric Eng 11:167–189

    Google Scholar 

  • Wang SY, Wang Y, Feng XJ, Zhai LM, Zhu GB (2011) Quantitative analyses of ammonia-oxidizing archaea and bacteria in the sediments of four nitrogen-rich wetlands in China. Appl Microbiol Biotechnol 90:779–787

    Article  CAS  Google Scholar 

  • Wang HT, Su JQ, Zheng TL, Yang XR (2015) Insights into the role of plant on ammonia-oxidizing bacteria and archaea in the mangrove ecosystem. J Soils Sediments 15:1212–1223

    Article  CAS  Google Scholar 

  • Wertz S, Leigh AKK, Grayston SJ (2012) Effects of long-term fertilization of forest soils on potential nitrification and on the abundance and community structure of ammonia oxidizers and nitrite oxidizers. FEMS Microbiol Ecol 79:142–154

    Article  CAS  Google Scholar 

  • Xing GX, Zhao X, Xiong ZQ, Yan XY, Xu H, Xie YX, Shi SL (2009) Nitrous oxide emission from paddy fields in China. Acta Ecol Sin 29:45–50

    Article  Google Scholar 

  • Yang SS, Liu CM, Lai CM, Liu YL (2003) Estimation of methane and nitrous oxide emission from paddy fields and uplands during 1990-2000 in Taiwan. Chemosphere 52:1295–1305

    Article  CAS  Google Scholar 

  • Zheng XH, Wang MX, Wang YS, Shen RX, Gou J, Li J, Jin JS, Li LT (2000) Impacts of soil moisture on nitrous oxide emission from croplands: a case study on rice-based agro-ecosystem in Southeast China. Chemosphere Global Change Sci 2:207–214

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Prof. Ron McLaren and Dr. Wenhua Wei for the help on this manuscript. This study was funded by the Natural Science Foundation of China (Grant Numbers 41330856, 41090282) and the Chinese Academy of Sciences (Grant Number XDB15020200).

Author information

Authors and Affiliations

  1. Key Laboratory of Agro-ecological Processes in Subtropical Region and Taoyuan Agro-ecosystem Research Station, Soil Molecular Ecology Section, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, 410125, China

    Zhenxing Zhang, Wenzhao Zhang, Huicui Yang, Rong Sheng, Wenxue Wei & Hongling Qin

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

    Zhenxing Zhang, Huicui Yang & Hongling Qin

Authors
  1. Zhenxing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wenzhao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Huicui Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rong Sheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wenxue Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hongling Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hongling Qin.

Additional information

Responsible editor: Philippe Garrigues

Electronic supplementary material

ESM 1

(DOCX 2092 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Z., Zhang, W., Yang, H. et al. Elevated N2O emission by the rice roots: based on the abundances of narG and bacterial amoA genes. Environ Sci Pollut Res 24, 2116–2125 (2017). https://doi.org/10.1007/s11356-016-7993-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-7993-2

Keywords

Search

Navigation