Advertisement

NirS-type N2O-producers and nosZ II-type N2O-reducers determine the N2O emission potential in farmland rhizosphere soils

  • Siyan Zhao
  • Jiemin Zhou
  • Dongdan Yuan
  • Weidong Wang
  • Liguang Zhou
  • Yanxia Pi
  • Guibing ZhuEmail author
Soils, Sec 5 • Soil and Landscape Ecology • Research Article
  • 16 Downloads

Abstract

Purpose

Denitrification process in agricultural fields is a large source of nitrous oxide (N2O) emitted to the atmosphere. The rhizosphere soils tend to be the hotspots of denitrification in agricultural soils. Recent studies have reported the important role of nosZ II in eliminating N2O. However, little was known about how these more recently discovered N2O-reducing microorganisms together with other N2O-producers affected the N2O emission in agricultural rhizosphere soils.

Materials and methods

Here, we compared the potential N2O production rate, the denitrification end-product ratio, and the denitrifier communities between rhizosphere and non-rhizosphere soils of two types of crops in winter and summer. The potential activities were measured by acetylene inhibition technique. QPCR analysis was used to quantify the functional genes. High-throughput sequencing and clone library were conducted to analyze the community structure of denitrifiers.

Results and discussion

The rhizosphere soils had a higher N2O production potential but lower denitrification end-product ratio (N2O/(N2O+N2)) than the non-rhizosphere soils. The potential N2O production rate was correlated to the nirS-bacteria abundance, especially in terms of the genus Azospirillum. The N2O/(N2O+N2) ratio showed a negative correlation with both the diversity and abundance of the nosZ II-type N2O-reducers.

Conclusions

Altogether, we propose that nirS-type N2O-producers and nosZ II-type N2O-reducers can affect the N2O emission in agricultural rhizosphere soils, and enhancement of diversity and abundance of nosZ II-type N2O-reducers may help with the N2O mitigation from upland crops.

Keywords

Farmland N2O-producers N2O-reducers nosZ II Rhizosphere soils 

Notes

Funding information

This research is financially supported by the National Natural Science Foundation of China (Nos. 41671471, 41322012, and 91851204), Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15020303), National Key R&D Program (2016YFA0602303), Local Innovative and Research Teams Project of Guangdong Pearl River Talents Program (2017BT01Z176), special fund from the State Key Joint Laboratory of Environment Simulation and Pollution Control (Research Center for Eco-environmental Sciences, Chinese Academy of Sciences) (18Z02ESPCR), Open Research Fund of Key Laboratory of Drinking Water Science and Technology, Chinese Academy of Sciences (16Z03KLDWST), and Program of the Youth Innovation Promotion Association (CAS).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

11368_2019_2395_MOESM1_ESM.docx (517 kb)
ESM 1 (DOCX 516 kb)

References

  1. Abell GC, Revill AT, Smith C, Bissett AP, Volkman JK, Robert SS (2010) Archaeal ammonia oxidizers and nirS-type denitrifiers dominate sediment nitrifying and denitrifying populations in a subtropical macrotidal estuary. ISME J 4:286–300CrossRefGoogle Scholar
  2. Ai C, Liang G, Wang X, Sun J, He P, Zhou W (2017) A distinctive root-inhabiting denitrifying community with high N2O/(N2O+N2) product ratio. Soil Biol Biochem 109:118–123CrossRefGoogle Scholar
  3. Bao S (2000) Soil and agricultural chemistry analysis. China Agriculture Press, BeijingGoogle Scholar
  4. Bardon C, Piola F, Bellvert F, Haichar F, Comte G, Meiffren G, Pommier T, Puijalon S, Tsafack N, Poly F (2014) Evidence for biological denitrification inhibition (BDI) by plant secondary metabolites. New Phytol 204:620–630CrossRefGoogle Scholar
  5. Beck H, Christensen S (1987) The effect of grass maturing and root decay on N2O production in soil. Plant Soil 103:269–273CrossRefGoogle Scholar
  6. 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 B Biol Sci 368:20130122CrossRefGoogle Scholar
  7. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefGoogle Scholar
  8. Conthe M, Wittorf L, Kuenen JG, Kleerebezem R, Hallin S, van Loosdrecht MC (2018) Growth yield and selection of nosZ clade II types in a continuous enrichment culture of N2O respiring bacteria. Env Microbiol Rep 10:239–244CrossRefGoogle Scholar
  9. Di Rienzi SC, Sharon I, Wrighton KC, Koren O, Hug LA, Thomas BC, Goodrich JK, Bell JT, Spector TD, Banfield JF (2013) The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria. Elife 2:e01102CrossRefGoogle Scholar
  10. Domeignoz-Horta L, Spor A, Bru D, Bizouard F, Leonard J, Philippot L (2015) The diversity of the N2O reducers matters for the N2O: N2 denitrification end-product ratio across an annual and a perennial cropping system. Front Microbiol 6:971CrossRefGoogle Scholar
  11. Domeignoz-Horta LA, Philippot L, Peyrard C, Bru D, Breuil MC, Bizouard F, Justes E, Mary B, Léonard J, Spor A (2017) Peaks of in situ N2O emissions are influenced by N2O producing and reducing microbial communities across arable soils. Glob Change Biol 24:360–370CrossRefGoogle Scholar
  12. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461CrossRefGoogle 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. Gobran GR, Clegg S (1996) A conceptual model for nutrient availability in the mineral soil-root system. Can J Soil Sci 76:125–131CrossRefGoogle Scholar
  15. Graf DR, Jones CM, Hallin S (2014) Intergenomic comparisons highlight modularity of the denitrification pathway and underpin the importance of community structure for N2O emissions. PLoS One 9:e114118CrossRefGoogle Scholar
  16. Hallin S, Philippot L, Löffler FE, Sanford RA, Jones CM (2017) Genomics and ecology of novel N2O-reducing microorganisms. Trends Microbiol 26:43–55CrossRefGoogle Scholar
  17. Henry S, Texier S, Hallet S, Bru D, Dambreville C, Cheneby D, Bizouard F, Germon J, Philippot L (2008) Disentangling the rhizosphere effect on nitrate reducers and denitrifiers: insight into the role of root exudates. Environ Microbiol 10:3082–3092CrossRefGoogle Scholar
  18. Hu H-W, Chen D, He J-Z (2015) Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates. FEMS Microbiol Rev 39:729–749CrossRefGoogle Scholar
  19. Ishii S, Ohno H, Tsuboi M, Otsuka S, Senoo K (2011) Identification and isolation of active N2O reducers in rice paddy soil. ISME J 5:1936–1945CrossRefGoogle Scholar
  20. Jones CM, Graf DR, Bru D, Philippot L, Hallin S (2013) The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink. ISME J 7:417–426CrossRefGoogle Scholar
  21. Jones CM, Spor A, Brennan FP, Breuil M-C, Bru D, Lemanceau P, Griffiths B, Hallin S, Philippot L (2014) Recently identified microbial guild mediates soil N2O sink capacity. Nat Clim Chang 4:801–805CrossRefGoogle Scholar
  22. Kong X, Duan Y, Schramm A, Eriksen J, Holmstrup M, Larsen T, Bol R, Petersen SO (2017) Mitigating N2O emissions from clover residues by 3, 4-dimethylpyrazole phosphate (DMPP) without adverse effects on the earthworm Lumbricus terrestris. Soil Biol Biochem 104:95–107CrossRefGoogle Scholar
  23. Liu XJ, Mosier AR, Halvorson AD, Reule CA, Zhang FS (2007) Dinitrogen and N2O emissions in arable soils: effect of tillage, N source and soil moisture. Soil Biol Biochem 39:2362–2370CrossRefGoogle Scholar
  24. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963CrossRefGoogle Scholar
  25. Mounier E, Hallet S, Cheneby D, Benizri E, Gruet Y, Nguyen C, Piutti S, Robin C, Slezack-Deschaumes S, Martin-Laurent F (2004) Influence of maize mucilage on the diversity and activity of the denitrifying community. Environ Microbiol 6:301–312CrossRefGoogle Scholar
  26. Payne WJ (1981) Denitrification. John Wiley & Sons Inc, New YorkGoogle Scholar
  27. Pell M, Stenberg B, Stenström J, Torstensson L (1996) Potential denitrification activity assay in soil-with or without chloramphenicol? Soil Biol Biochem 28:393–398CrossRefGoogle Scholar
  28. Philippot L, Andert J, Jones CM, Bru D, Hallin S (2011) Importance of denitrifiers lacking the genes encoding the nitrous oxide reductase for N2O emissions from soil. Glob Chang Biol 17:1497–1504CrossRefGoogle Scholar
  29. Philippot L, Hallin S, Schloter M (2007) Ecology of denitrifying prokaryotes in agricultural soil. Adv Agron 96:249–305CrossRefGoogle Scholar
  30. Robertson G, Vitousek P, Matson P, Tiedje J (1987) Denitrification in a clearcut Loblolly pine (Pinus taeda L.) plantation in the southeastern US. Plant Soil 97:119–129CrossRefGoogle Scholar
  31. Søvik A, Kløve B (2007) Emission of N2O and CH4 from a constructed wetland in southeastern Norway. Sci Total Environ 380:28–37CrossRefGoogle Scholar
  32. Saarenheimo J, Rissanen AJ, Arvola L, Nykänen H, Lehmann MF, Tiirola M (2015) Genetic and environmental controls on nitrous oxide accumulation in lakes. PLoS One 10:e0121201CrossRefGoogle Scholar
  33. Samad MS, Biswas A, Bakken LR, Clough TJ, De Klein CA, Richards KG, Lanigan GJ, Morales SE (2016) Phylogenetic and functional potential links pH and N2O emissions in pasture soils. Sci Rep 6:35990CrossRefGoogle Scholar
  34. Sanford RA, Wagner DD, Wu Q, Chee-Sanford JC, Thomas SH, Cruz-García C, Rodríguez G, Massol-Deyá A, Krishnani KK, Ritalahti KM (2012) Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. P Natl Acad Sci USA 109:19709–19714CrossRefGoogle Scholar
  35. Scheer C, Wassmann R, Butterbach-Bahl K, Lamers JP, Martius C (2009) The relationship between N2O, NO, and N2 fluxes from fertilized and irrigated dryland soils of the Aral Sea Basin, Uzbekistan. Plant Soil 314:273–283CrossRefGoogle Scholar
  36. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefGoogle Scholar
  37. Seitzinger S, Harrison JA, Böhlke J, Bouwman A, Lowrance R, Peterson B, Tobias C, Drecht GV (2006) Denitrification across landscapes and waterscapes: a synthesis. Ecol Appl 16:2064–2090CrossRefGoogle Scholar
  38. Sun L, Lu Y, Kronzucker HJ, Shi W (2016) Quantification and enzyme targets of fatty acid amides from duckweed root exudates involved in the stimulation of denitrification. J Plant Physiol 198:81–88CrossRefGoogle Scholar
  39. Syakila A, Kroeze C (2011) The global nitrous oxide budget revisited. Greenhouse Gas Meas Manage 1:17–26CrossRefGoogle Scholar
  40. Truu M, Ostonen I, Preem J-K, Lõhmus K, Nõlvak H, Ligi T, Rosenvald K, Parts K, Kupper P, Truu J (2017) Elevated air humidity changes soil bacterial community structure in the silver birch stand. Front Microbiol 8:557CrossRefGoogle Scholar
  41. Wallenstein MD, Myrold DD, Firestone M, Voytek M (2006) Environmental controls on denitrifying communities and denitrification rates: insights from molecular methods. Ecol Appl 16:2143–2152CrossRefGoogle Scholar
  42. Wang H, Marshall CW, Cheng M, Xu H, Li H, Yang X, Zheng T (2017) Changes in land use driven by urbanization impact nitrogen cycling and the microbial community composition in soils. Sci Rep 7:44049CrossRefGoogle Scholar
  43. Wang Q, Quensen JF, Fish JA, Lee TK, Sun Y, Tiedje JM, Cole JR (2013) Ecological patterns of nifH genes in four terrestrial climatic zones explored with targeted metagenomics using FrameBot, a new informatics tool. MBio 4:e00592–e00513Google Scholar
  44. Ye X, Li J, Wang Y-h, E-m L, Li R-x YQ, B-x C (2005) Characterization of emissions of nitrous oxide from soils of typical crop fields in North China Plain. JAES 24:1186–1191Google Scholar
  45. Yoon S, Nissen S, Park D, Sanford RA, Löffler FE (2016) Nitrous oxide reduction kinetics distinguish bacteria harboring clade I versus clade II NosZ. Appl Environ Microbiol: AEM:00409–00416Google Scholar
  46. Zhao S, Wang Q, Zhou J, Yuan D, Zhu G (2018) Linking abundance and community of microbial N2O-producers and N2O-reducers with enzymatic N2O production potential in a riparian zone. Sci Total Environ 642:1090–1099CrossRefGoogle Scholar
  47. Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol R 61:533–616Google Scholar
  48. Zumft WG, Kroneck PM (2006) Respiratory transformation of nitrous oxide (N2O) to dinitrogen by Bacteria and Archaea. Adv Microb Physiol 52:107–227CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Drinking Water Science and Technology, Research Center for Eco-Environmental SciencesChinese Academy of SciencesBeijingChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.School of Municipal and Environmental EngineeringJilin Jianzhu UniversityChangchunChina

Personalised recommendations