Ammonia-oxidation as an engine to generate nitrous oxide in an intensively managed calcareous Fluvo-aquic soil

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Huang, Tao ^a   Gao, Bing ^a   Hu, Xiao Kang ^a   Lu, Xing ^a   Well, Reinhard ^b   Christie, Peter ^a   Bakken, Lars R ^c   Ju, Xiao Tang ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b THÜNEN INSTITUTE OF CLIMATE SMART AGRICULTURE   (Germany)

^c NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84893836879     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep03950     Document Type: Article

References (55)

1. Solomon, S. et al. in Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds Solomon S. et al) 33-34 (Cambridge University Press, Cambridge, 2007
2. Davidson, E. A. The contribution of manure and fertilizer nitrogen to atmospheric nitrous oxide since 1860. Nature Geosci. 2, 659-662 (2009
3. Butterbach-Bahl, K., Baggs, E. M., Dannenmann, M., Kiese, R. & Zechmeister- Boltenstern, S. Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Philos. Trans. R. Soc. B-Biol. Sci. 368, 1-13 (2013
4. Ju, X. T. et al. Reducing environmental risk by improving N management in intensive Chinese agricultural systems. Proc. Natl. Acad. Sci. U. S. A. 106, 3041-3046 (2009
5. Braker, G.& Conrad, R. Diversity, structure, and size ofN2O-producing microbial communities in soils-whatmatters for their functioning? Adv. Appl. Microbiol. 75, 33-70 (2011
6. Baggs, E. M. Soil microbial sources of nitrous oxide: recent advances in knowledge, emerging challenges and future direction. Curr. Opin. Environ. Sustain. 3, 321-327 (2011
7. Wrage, N., Velthof, G. L., van Beusichem, M. L. & Oenema, O. Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol. Biochem. 33, 1723-1732 (2001 (Pubitemid 32961521)
8. Samarkin, V. A. et al. Abiotic nitrous oxide emission from the hypersaline Don Juan Pond in Antarctica. Nature Geosci. 3, 341-344 (2010
9. Robertson, G. P. inMineral Nutrients in Tropical Forest and Savanna Ecosystems (eds Proctor J.) 55-69 (Blackwell Scientific, London, 1989
10. Groffman, P.M. et al.Methods for measuring denitrification: Diverse approaches to a difficult problem. Ecol. Appl. 16, 2091-2122 (2006 (Pubitemid 44917573)
11. Well, R., Flessa, H., Lu, X., Ju, X. & Ro¨emheld, V. Isotopologue ratios of N2O emitted from microcosms with NH4 1 fertilized arable soils under conditions favoring nitrification. Soil Biol. Biochem. 40, 2416-2426 (2008
12. Wan, Y. J. et al. Gross nitrogen transformations and related nitrous oxide emissions in an intensively used calcareous soil. Soil Sci. Soc. Am. J. 73, 102-112 (2009
13. Ju, X. T. et al. Processes and factors controlling N2O production in an intensively managed low carbon calcareous soil under sub-humid monsoon conditions. Environ. Pollut. 159, 1007-1016 (2011
14. Bao, Q. L. et al. Response of nitrous oxide and corresponding bacteria to managements in an agricultural soil. Soil Sci. Soc. Am. J. 76, 130-141 (2012
15. Hu, X. K. et al. Greenhouse gas emissions from a wheat-maize double cropping system with different nitrogen fertilization regimes. Environ. Pollut. 176, 198-207 (2013
16. Molstad, L., Do¨rsch, P. & Bakken, L. R. Robotized incubation system for monitoring gases (O2, NO,N2ON2) in denitrifying cultures. J. Microbiol. Methods 71, 202-211 (2007 (Pubitemid 350151512)
17. Dobbie, K. E.&Smith, K.A.Nitrous oxide emission factors for agricultural soils in Great Britain: the impact of soil water-filled pore space and other controlling variables. Glob. Change Biol. 9, 204-218 (2003 (Pubitemid 36290352)
18. Parkin, T. B. & Tiedje, J. M. Application of a soil core method to investigate the effect of oxygen concentration on denitrification. Soil Biol. Biochem. 16, 331-334 (1984
19. Ostrom, N. E. & Ostrom, P. H. in Handbook of Environmental Isotope Geochemistry, Advances in Isotope Geochemistry (eds Baskaran M.) 453-476 (Springer, Berlin, 2011
20. Sutka, R. L. et al. Distinguishing nitrous oxide production from nitrification and denitrification on the basis of isotopomer abundances. Appl. Environ. Microbiol. 72, 638-644 (2006
21. Di, H. J. et al. Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nature Geosci. 2, 621-624 (2009
22. Rotthauwe, J. H., Witzel, K. P. & Liesack, W. 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 (1997 (Pubitemid 27524201)
23. Kumar, S., Tamura, K. & Nei, M. MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5, 150-163 (2004
24. Szukics, U. et al. Nitrifiers and denitrifiers respond rapidly to changed moisture and increasing temperature in a pristine forest soil. FEMS Microbiol. Ecol. 72, 395-406 (2010
25. Braker, G., Fesefeldt, A. &Witzel, K. P. Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl. Environ. Microbiol. 64, 3769-3775 (1998 (Pubitemid 28462971)
26. Henry, S. et al. Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. J. Microbiol. Methods 59, 327-335 (2004 (Pubitemid 39370795)
27. Ma, W. K., Bedard-Haughn, A., Siciliano, S. D. & Farrell, R. E. Relationship between nitrifier and denitrifier community composition and abundance in predicting nitrous oxide emissions from ephemeral wetland soils. Soil Biol. Biochem. 40, 1114-1123 (2008
28. Frame, C. H. & Casciotti, K. L. Biogeochemical controls and isotopic signatures of nitrous oxide production by a marine ammonia-oxidizing bacterium. Biogeosciences 7, 2695-2709 (2010
29. Ostrom, N. E. et al. Isotopologue effects during N2O reduction in soils and in pure cultures of denitrifiers. J. Geophys. Res. 112, G02005 (2007
30. Park, S. et al. Can N2O stable isotopes and isotopomers be useful tools to characterize sources and microbial pathways of N2O production and consumption in tropical soils? Global Biogeochem. Cycles 25, GB1001 (2011
31. Kool, D. M.,Wrage, N., Oenema, O., Dolfing, J. & Van Groenigen, J. W. Oxygen exchange between (de)nitrification intermediates and H2O and its implications for source determination of NO3 2 and N2O: a review. Rapid Commun. Mass Spectrom. 21, 3569-3578 (2007 (Pubitemid 350124624)
32. Casciotti, K. L., Buchwald, C., Santoro, A. E. & Frame, C. in Methods in Enzymology: Research on Nitrification and Related Processes, Part A (eds Klotz M. G.) 253-280 (Academic Press, San Diego, 2011
33. Xia, W. W. et al. Autotrophic growth of nitrifying community in an agricultural soil. ISME J. 5, 1226-1236 (2011
34. Santoro, A. E., Buchwald, C., McIlvin, M. R. & Casciotti, K. L. Isotopic signature of N2O produced by marine ammonia-oxidizing archaea. Science 333, 1282-1285 (2011
35. Bremer, C. et al. Impact of plant functional group, plant species, and sampling time on the composition of nirK-Type denitrifier communities in soil. Appl. Environ. Microbiol. 73, 6876-6884 (2007 (Pubitemid 350076806)
36. Philippot, L., Piutti, S., Martin-Laurent, F., Hallet, S. & Germon, J. C. Molecular analysis of the nitrate-reducing community from unplanted and maize-planted soils. Appl. Environ. Microbiol. 68, 6121-6128 (2002 (Pubitemid 36342448)
37. Guo, G. X., Deng, H., Qiao, M., Mu, Y. J. & Zhu, Y. G. Effect of pyrene on denitrification activity and abundance and composition of denitrifying community in an agricultural soil. Environ. Pollut. 159, 1886-1895 (2011
38. Yoshida, M., Ishii, S., Otsuka, S. & Senoo, K. Temporal shifts in diversity and quantity of nirS and nirK in a rice paddy field soil. Soil Biol. Biochem. 41, 2044-2051 (2009
39. Ju, X. T., Kou, C. L., Zhang, F. S. & Christie, P. Nitrogen balance and groundwater nitrate contamination: Comparison among three intensive cropping systems on the North China Plain. Environ. Pollut. 143, 117-125 (2006
40. Ju, X. T., Liu, X. J., Zhang, F. S. & Roelcke, M. Nitrogen fertilization, soil nitrate accumulation, and policy recommendations in several agricultural regions of China. Ambio 33, 300-305 (2004 (Pubitemid 39123414)
41. Zhu, X., Burger, M.,Doane, T. A.&Horwath, W. R. Ammonia oxidation pathways and nitrifier denitrification are significant sources of N2O and NO under low oxygen availability. Proc. Natl. Acad. Sci. U. S. A. 110, 6328-6333 (2013
42. Sexstone, A. J., Revsbech,N. P., Parkin, T. B.&Tiedje, J. M. Direct measurement of oxygen profiles and denitrification rates in soil aggregates. Soil Sci. Soc. Am. J. 49, 645-651 (1985
43. Smith, K. A. The potential for feedback effects induced by global warming on emissions of nitrous oxide by soils. Glob. Change Biol. 3, 327-338 (1997
44. Tiedje, J. M., Sexstone, A. J., Parkin, T. B.&Revsbech, N. P. Anaerobic processes in soil. Plant Soil 76, 197-212 (1984
45. Hooper, A. B. A nitrite-reducing enzyme from Nitrosomonas europaea. Preliminary characterization with hydroxylamine as electron donor. Biochim. Biophys. Acta 162, 49-65 (1968
46. Ritchie, G. A. & Nicholas, D. J. Identification of the sources of nitrous oxide produced by oxidative and reductive processes in Nitrosomonas europaea. Biochem. J. 126, 1181-1191 (1972
47. Shaw, L. J. et al. Nitrosospira spp. can produce nitrous oxide via a nitrifier denitrification pathway. Environ. Microbiol. 8, 214-222 (2006
48. Kool, D. M. et al. Nitrifier denitrification can be a source of N2O from soil: a revised approach to the dual-isotope labellingmethod. Eur. J. Soil Sci. 61, 759-772 (2010
49. Kool, D. M.,Dolfing, J., Wrage, N.&Van Groenigen, J.W.Nitrifier denitrification as a distinct and significant source of nitrous oxide from soil. Soil Biol. Biochem. 43, 174-178 (2011
50. Leininger, S. et al. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806-809 (2006 (Pubitemid 44258909)
51. Stahl, D. A. & de la Torre, J. R. Physiology and diversity of ammonia-oxidizing archaea. Annu. Rev. Microbiol. 66, 83-101 (2012
52. Prosser, J. I. & Nicol, G. W. Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol. 20, 523-531 (2012
53. Carrasco, D., Fernandez-Valiente, E., Ariosa, Y. & Quesada, A. Measurement of coupled nitrification-denitrification in paddy fields affected by Terrazole, a nitrification inhibitor. Biol. Fertil. Soils 39, 186-192 (2004 (Pubitemid 38285679)
54. dosSantos, V., Bruijnse, M., Tramper, J. &Wijffels, R. H. The magic bead concept: An integrated approach to nitrogen removal with co-immobilized microorganisms. Appl. Microbiol. Biotechnol. 45, 447-453 (1996
55. Kremen, A., Bear, J., Shavit, U.&Shaviv, A. Model demonstrating the potential for coupled nitrification denitrification in soil aggregates. Environ. Sci. Technol. 39, 4180-4188 (2005 (Pubitemid 40770248)