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Biology and Fertility of Soils

, Volume 53, Issue 8, pp 885–898 | Cite as

Nitrous oxide (N2O)-reducing denitrifier-inoculated organic fertilizer mitigates N2O emissions from agricultural soils

  • Nan Gao
  • Weishou Shen
  • Estefania Camargo
  • Yutaka Shiratori
  • Tomoyasu Nishizawa
  • Kazuo Isobe
  • Xinhua He
  • Keishi Senoo
Original Paper

Abstract

The only known sink for nitrous oxide (N2O) is biochemical reduction to dinitrogen (N2) by N2O reductase (N2OR). We hypothesized that the application of N2O-reducing denitrifier-inoculated organic fertilizer could enhance soil N2O consumption while the disruption of nosZ genes could result in inactivation of N2O consumption. To test such hypotheses, a denitrifier-inoculated granular organic fertilizer was applied to both soil microcosms and fields. Of 41 denitrifier strains, 38 generated 30N2 in the end products of denitrification (30N2 and 46N2O) after the addition of Na15NO3 in culture condition, indicating their high N2O reductase activities. Of these 41 strains, 18 were screened in soil microcosms after their inoculation into the organic fertilizer, most of which were affiliated with Azospirillum and Herbaspirillum. These 18 strains were nutritionally starved to improve their survival in soil, and 14 starved and/or non-starved strains significantly decreased N2O emissions in soil microcosms. However, the N2O emission had not been decreased in soil microcosms after inoculating with a nosZ gene-disruptive strain, suggesting that N2O reductase activity might be essential for N2O consumption. Although the decrease of N2O was not significant at field scales, the application of organic fertilizer inoculated with Azospirillum sp. TSH100 and Herbaspirillum sp. UKPF54 had decreased the N2O emissions by 36.7% in Fluvisol and 23.4% in Andosol in 2014, but by 21.6% in Andosol in 2015 (H. sp. UKPF54 only). These results suggest that the application of N2O-reducing denitrifier-inoculated organic fertilizer may enhance N2O consumption or decrease N2O emissions in agricultural soils.

Keywords

Climate change Greenhouse gas Microbiological manipulation Mitigation technology Nitrous oxide consumption and sink Nitrous oxide reductase 

Notes

Acknowledgements

We thank Shigeto Otsuka for his helpful discussion and Chie Hayakawa for her help with gas sampling in the fields. We also thank the technical staffs from the Niigata Agricultural Research Institute and the Institute for Sustainable Agro-ecosystem Services, The University of Tokyo for their assistance with field work. This study was supported by the Japan Society for the Promotion of Science through a Postdoctoral Fellowship (14F04390), the Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry, and the Science and Technology Research Promotion Program for Agriculture, Forestry, Fisheries and Food Industry (26037B and 27004C), Japan.

Supplementary material

374_2017_1231_MOESM1_ESM.docx (17 kb)
Table S1 (DOCX 17 kb).
374_2017_1231_MOESM2_ESM.docx (21 kb)
Table S2 (DOCX 20 kb).
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Figure S1 (DOCX 3338 kb).
374_2017_1231_MOESM4_ESM.docx (213 kb)
Figure S2 (DOCX 212 kb).

References

  1. Abdalla M, Jones M, Smith P, Williams M (2009) Nitrous oxide fluxes and denitrification sensitivity to temperature in Irish pasture soils. Soil Use Manage 25:376–388CrossRefGoogle Scholar
  2. Aguilera E, Lassaletta L, Sanz-Cobena A, Garnier J, Vallejo A (2013) The potential of organic fertilizers and water management to reduce N2O emissions in Mediterranean climate cropping systems. A review. Agric Ecosyst Environ 164:32–52CrossRefGoogle Scholar
  3. Akiyama H, Hoshino YT, Itakura M, Shimomura Y, Wang Y, Yamamoto A, Tago K, Nakajima Y, Minamisawa K, Hayatsu M (2016) Mitigation of soil N2O emission by inoculation with a mixed culture of indigenous Bradyrhizobium diazoefficiens. Sci Rep 6:32869CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ashida N, Ishii S, Hayano S, Tago K, Tsuji T, Yoshimura Y, Otsuka S, Senoo K (2010) Isolation of functional single cells from environments using a micromanipulator: application to study denitrifying bacteria. Appl Microbiol Biotechnol 85:1211–1217CrossRefPubMedGoogle Scholar
  5. Banerjee S, Helgasonb B, Wang LF, Winsley T, Ferrari BC, Siciliano SD (2016) Legacy effects of soil moisture on microbial community structure and N2O emissions. Soil Biol Biochem 95:40–50CrossRefGoogle Scholar
  6. Blagodatsky S, Smith P (2012) Soil physics meets soil biology: towards better mechanistic prediction of greenhouse gas emissions from soil. Soil Biol Biochem 47:78–92CrossRefGoogle Scholar
  7. Braker G, Fesefeldt A, Witzel KP (1998) Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl Environ Microbiol 64:3769–3775PubMedPubMedCentralGoogle Scholar
  8. Butterbach-Bahl K, Baggs EM, Dannenmann M, Kiese R, Zechmeister-Boltenstern S (2013) Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Philos Trans R Soc Lond Ser B Biol Sci 368:20130122CrossRefGoogle Scholar
  9. Cai Y, Chang SX, Ma B, Bork EW (2016) Watering increased DOC concentration but decreased N2O emission from a mixed grassland soil under different defoliation regimes. Biol Fertil Soils 52:987–996CrossRefGoogle Scholar
  10. De Rosa D, Rowlings DW, Biala J, Scheer C, Basso B, McGree J, Grace PR (2016) Effect of organic and mineral N fertilizers on N2O emissions from an intensive vegetable rotation. Biol Fertil Soils 52:895–908CrossRefGoogle Scholar
  11. Diacono M, Montemurro F (2010) Long-term effects of organic amendments on soil fertility. A review. Agron Sustain Dev 30:401–422CrossRefGoogle Scholar
  12. Felgate H, Giannopoulos G, Sullivan MJ, Gates AJ, Clarke TA, Baggs E, Rowley G, Richardson DJ (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. Environ Microbiol 14:1788–1800CrossRefPubMedGoogle Scholar
  13. Friedl J, Scheer C, Rowlings DW, McIntosh HV, Strazzabosco A, Warner DI, Grace PR (2016) Denitrification losses from an intensively managed sub-tropical pasture—impact of soil moisture on the partitioning of N2 and N2O emissions. Soil Biol Biochem 92:58–66CrossRefGoogle Scholar
  14. Gao N, Shen WS, Kakuta H, Tanaka N, Fujiwara T, Nishizawa T, Takaya N, Nagamine T, Isobe K, Otsuka S, Senoo K (2016) Inoculation with nitrous oxide (N2O)-reducing denitrifier strains simultaneously mitigates N2O emission from pasture soil and promotes growth of pasture plants. Soil Biol Biochem 97:83–91CrossRefGoogle Scholar
  15. Greenhouse Gas Inventory Office of Japan (GIO), Center for Global Environmental Research (CGER), National Institute for Environmental Studies (NIES) (2012) National Greenhouse Gas Inventory Report of Japan 2012. http://www-gio.nies.go.jp/aboutghg/nir/2012/NIR-JPN-2012-v3.0E.pdf
  16. Gu YH, Mazzola M (2001) Impact of carbon starvation on stress resistance, survival in soil habitats and biocontrol ability of Pseudomonas putida strain 2C8. Soil Biol Biochem 33:1155–1162CrossRefGoogle Scholar
  17. Hayakawa A, Akiyama H, Sudo S, Yagi K (2009) N2O and NO emissions from an Andisol field as influenced by pelleted poultry manure. Soil Biol Biochem 41:521–529CrossRefGoogle Scholar
  18. Hayatsu M, Tago K, Saito M (2008) Various players in the nitrogen cycle: diversity and functions of the microorganisms involved in nitrification and denitrification. Soil Sci Plant Nutr 54:33–45CrossRefGoogle Scholar
  19. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP (1998) A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77–86CrossRefPubMedGoogle Scholar
  20. Hu HW, Chen DL, He JZ (2015) Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates. FEMS Microbiol Rev 39:729–749CrossRefPubMedGoogle Scholar
  21. IPCC (2013) Observations: atmosphere and surface. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, pp 159–254Google Scholar
  22. Ishii S, Ohno H, Tsuboi M, Otsuka S, Senoo K (2011) Identification and isolation of active N2O reducers in rice paddy soil. ISME J 5:1936–1945CrossRefPubMedPubMedCentralGoogle Scholar
  23. Itakura M, Uchida Y, Akiyama H, Hoshino YT, Shimomura Y, Morimoto S, Tago K, Wang Y, Hayakawa C, Uetake Y, Sánchez C, Eda S, Hayatsu M, Minamisawa K (2013) Mitigation of nitrous oxide emissions from soils by Bradyrhizobium japonicum inoculation. Nat Clim Chang 3:208–212CrossRefGoogle Scholar
  24. Jones CM, Graf DRH, Bru D, Philippot L, Hallin S (2013) The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink. ISME J 7:417–426CrossRefPubMedGoogle Scholar
  25. Jones CM, Spor A, Brennan FP, Breuil MC, Bru D, Lemanceau P, Griffiths B, Sara Hallin S, Philippot L (2014) Recently identified microbial guild mediates soil N2O sink capacity. Nat Clim Chang 4:801–805CrossRefGoogle Scholar
  26. Klein CAM, Harvey MJ (2012) Nitrous oxide chamber methodology guidelines. Ministry of Primary Industries, Wellington, New ZealandGoogle Scholar
  27. Liu R, Hayden HL, Suter H, Hu HW, Lam SK, He JZ, Mele PM, Chen DL (2017) The effect of temperature and moisture on the source of N2O and contributions from ammonia oxidizers in an agricultural soil. Biol Fertil Soils 53:141–152CrossRefGoogle Scholar
  28. Luo J, de Klein CAM, Ledgard SF, Saggar S (2010) Management options to reduce nitrous oxide emissions from intensively grazed pastures: a review. Agric Ecosyst Environ 136:282–291CrossRefGoogle Scholar
  29. Ma L, Shan J, Yan XY (2015) Nitrite behavior accounts for the nitrous oxide peaks following fertilization in a fluvo-aquic soil. Biol Fertil Soils 51:563–572CrossRefGoogle Scholar
  30. Minick KJ, Pandey CB, Fox TR, Subedi S (2016) Dissimilatory nitrate reduction to ammonium and N2O flux: effect of soil redox potential and N fertilization in loblolly pine forests. Biol Fertil Soils 52:601–614CrossRefGoogle Scholar
  31. Nishizawa T, Quan AH, Kai A, Tago K, Ishii S, Shen WS, Isobe K, Otsuka S, Senoo K (2014) Inoculation with N2-generating denitrifier strains mitigates N2O emission from agricultural soil fertilized with poultry manure. Biol Fertil Soils 50:1001–1007CrossRefGoogle Scholar
  32. Nishizawa T, Tago K, Uei Y, Ishii S, Isobe K, Otsuka S, Senoo K (2012) Advantages of functional single-cell isolation method over standard agar plate dilution method as a tool for studying denitrifying bacteria in rice paddy soil. AMB Express 2:50CrossRefPubMedPubMedCentralGoogle Scholar
  33. Nishizawa T, Uei Y, Tago K, Isobe K, Otsuka S, Senoo K (2013) Taxonomic composition of denitrifying bacterial isolates is different among three rice paddy field soils in Japan. Soil Sci Plant Nutr 59:305–310CrossRefGoogle Scholar
  34. Qu Z, Wang JG, Almøy T, Bakken LR (2014) Excessive use of nitrogen in Chinese agriculture results in high N2O/(N2O + N2) product ratio of denitrification, primarily due to acidification of the soils. Glob Chang Biol 20:1685–1698CrossRefPubMedPubMedCentralGoogle Scholar
  35. Reay DS, Davidson EA, Smith KA, Smith P, Melillo JM, Dentener F, Crutzen PJ (2012) Global agriculture and nitrous oxide emissions. Nat Clim Chang 2:410–416CrossRefGoogle Scholar
  36. Rich JJ, Heichen SS, Bottomley PJ, Cromack K Jr, Myrold DD (2003) Community composition and functioning of denitrifying bacteria from adjacent meadow and forest soils. Appl Environ Microbiol 69:5974–5982CrossRefPubMedPubMedCentralGoogle Scholar
  37. Sanford RA, Wagner DD, Wu QZ, Chee-Sanford JC, Thomas SH, Cruz-García C, Rodríguez G, Massol-Deyá A, Krishnani KK, Ritalahti KM, Nissen S, Konstantinidis KT, Löffler FE (2012) Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proc Natl Acad Sci U S A 109:19709–19714CrossRefPubMedPubMedCentralGoogle Scholar
  38. Santasup C, Senoo K, Bhromsiri A, Shutsrirung A, Tanaka A, Obata H (2001) Improved survival of nutrient-starved cells of Rhizobium tropici CIAT899 in acid soil associated with high Al3+ and Mn2+ contents. Soil Sci Plant Nutr 47:559–567CrossRefGoogle Scholar
  39. Shcherbak L, Millar N, Robertson GP (2014) Global metaanalysis of the nonlinear response of soil nitrous oxide (N2O) emissions to fertilizer nitrogen. Proc Natl Acad Sci U S A 111:9199–9204CrossRefPubMedPubMedCentralGoogle Scholar
  40. Sullivan MJ, Gates AJ, Appia-Ayme C, Rowley G, Richardson DJ (2013) Copper control of bacterial nitrous oxide emission and its impact on vitamin B12-dependent metabolism. Proc Natl Acad Sci U S A 110:19926–19931CrossRefPubMedPubMedCentralGoogle Scholar
  41. Tago K, Ishii S, Nishizawa T, Otsuka S, Senoo K (2011) Phylogenetic and functional diversity of denitrifying bacteria isolated from various rice paddy and rice-soybean rotation fields. Microbes Environ 26:30–35CrossRefPubMedGoogle Scholar
  42. Thomson AJ, Giannopoulos G, Pretty J, Baggs EM, Richardson DJ (2012) Biological sources and sinks of nitrous oxide and strategies to mitigate emissions. Philos Trans R Soc Lond Ser B Biol Sci 367:1157–1168CrossRefGoogle Scholar
  43. Throbäck 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 49:401–417CrossRefPubMedGoogle Scholar
  44. Uchida Y, Wang Y, Akiyama H, Nakajima Y, Hayatsu M (2014) Expression of denitrification genes in response to a waterlogging event in a Fluvisol and its relationship with large nitrous oxide pulses. FEMS Microbiol Ecol 88:407–423CrossRefPubMedGoogle Scholar
  45. Van Kessel C, Venterea R, Six J, Adviento-Borbe MA, Linquist B, Groenigen KJV (2013) Climate, duration, and N placement determine N2O emissions in reduced tillage systems: a meta-analysis. Glob Chang Biol 19:33–44CrossRefPubMedGoogle Scholar
  46. Van Overbeek LS, Eberl L, Givskov M, Molin S, van Elsas JD (1995) Survival of, and induced stress resistance in, carbon-starved Pseudomonas fluorescens cells residing in soil. Appl Environ Microbiol 61:4202–4208PubMedPubMedCentralGoogle Scholar
  47. Wei W, Isobe K, Shiratori Y, Nishizawa T, Ohte N, Otsuka S, Senoo K (2014) N2O emission from cropland field soil through fungal denitrification after surface applications of organic fertilizer. Soil Biol Biochem 69:157–167CrossRefGoogle Scholar
  48. Whitehead D, Edwards GR (2015) Assessment of the application of gibberellins to increase productivity and reduce nitrous oxide emissions in grazed grassland. Agric Ecosyst Environ 207:40–50CrossRefGoogle Scholar
  49. Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:533–616PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Nan Gao
    • 1
  • Weishou Shen
    • 2
    • 3
  • Estefania Camargo
    • 4
  • Yutaka Shiratori
    • 5
  • Tomoyasu Nishizawa
    • 6
  • Kazuo Isobe
    • 3
  • Xinhua He
    • 7
  • Keishi Senoo
    • 3
  1. 1.National Engineering Research Center for Biotechnology and School of Biotechnology and Pharmaceutical EngineeringNanjing Tech UniversityNanjingChina
  2. 2.School of Environmental Science and EngineeringNanjing University of Information Science and TechnologyNanjingChina
  3. 3.Department of Applied Biological Chemistry, Graduate School of Agricultural and Life SciencesThe University of TokyoTokyoJapan
  4. 4.Department of Soil ScienceFederal University of Rio Grande do SulRio Grande do SulBrazil
  5. 5.Niigata Agricultural Research InstituteNiigataJapan
  6. 6.Department of Food and Life Sciences, College of AgricultureIbaraki UniversityIbarakiJapan
  7. 7.Centre of Excellence for Soil Biology, College of Resources and EnvironmentSouthwest UniversityChongqingChina

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