Abstract
Background
Replacing synthetic fertilizers by biological nitrogen fixation (BNF) is regarded as an environmentally sound practice, but some diazotrophic bacteria are capable of emitting N2O by denitrification. The ability to use nitrate represents an ecological advantage for the survival of some microorganisms under O2-limiting conditions, but may contribute to increased N2O emissions.
Scope
The importance of denitrification performed by N2-fixing bacteria used as inoculants in South America is discussed, especially the possibility of these bacteria act as N2O source or sink.
Conclusions
There is no doubt of the importance of BNF as a sustainable N source for plants. Through genome investigation, we demonstrated that some strains widely used as inoculants for BNF harbor the entire denitrification pathway to reduce nitrate to N2. Others contain none, or only some of the denitrification genes, resulting in complete absence of denitrification or production of intermediates such as NO2−, NO or N2O. Evidence of differential effects of bacterial strains on soil N2O were reported, but more studies are still needed to affirm crop inoculation can be a driver for source or sink of this gas. Finally, considerations were made about BNF as an indispensable resource to indirectly mitigate greenhouse gas emissions in agroecosystems.
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References
Akiyama H, Morimoto S, Hayatsu M, Hayakawa A, Sudo S, Yagi K (2013) Nitrification, ammonia-oxidizing communities, and N2O and CH4 fluxes in an imperfectly drained agricultural field fertilized with coated urea with and without dicyandiamide. Biol Fertil Soils 49:213–223. https://doi.org/10.1007/s00374-012-0713-2
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 6:32869. https://doi.org/10.1038/srep32869
Azziz G, Monza J, Etchebehere C, Irisarri P (2017) nirS- and nirK-type denitrifier communities are differentially affected by soil type, rice cultivar and water management. Eur J Soil Biol 7:20–28. https://doi.org/10.1016/j.ejsobi.2016.11.003
Baggs EM, Rees RM, Smith KA, Vinten AJA (2000) Nitrous oxide emission from soils after incorporating crop residues. Soil Use Manag 16:82–87. https://doi.org/10.1111/j.1475-2743.2000.tb00179.x
Barken LR, Børresen T, Njøs A (1987) Effect of soil compaction by tractor traffic on soil structure, denitrification, and yield of wheat (Triticum aestivum L.). J Soil Sci 38:541–552. https://doi.org/10.1111/j.1365-2389.1987.tb02289.x
Bayer C, Gomes J, Zanatta JA, Vieira FCB, MdC P, Dieckow J, Six J (2015) Soil nitrous oxide emissions as affected by long-term tillage, cropping systems and nitrogen fertilization in Southern Brazil. Soil Tillage Res 146:213–222. https://doi.org/10.1016/j.still.2014.10.011
Bedmar EJ, Bueno E, Correa D, Torres MJ, Delgado MJ, Mesa S (2013) Ecology of denitrification in soils and plant-associated Bacteria. In: Beneficial Plant-microbial Interactions. CRC Press, pp 165–182. https://doi.org/10.1201/b15251-9
Bleakley BH, Tiedje JM (1982) Nitrous oxide production by organisms other than Nitrifiers or Denitrifiers. Appl Environ Microbiol 44:1342–1348
Bouwman AF (1996) Direct emission of nitrous oxide from agricultural soils. Nutr Cycl Agroecosyst 46:53–70. https://doi.org/10.1007/bf00210224
Brasil. Ministério da Agricultura, Pecuária e Abastecimento 2012. Plano setorial de mitigação e de adaptação às mudanças climáticas para a consolidação de uma economia de baixa emissão de carbono na agricultura : plano ABC (Agricultura de Baixa Emissão de Carbono) / Ministério da Agricultura, Pecuária e Abastecimento, Ministério do Desenvolvimento Agrário, coordenação da Casa Civil da Presidência da República. – Brasília : MAPA/ACS. 173 phttp://www.agricultura.gov.br/assuntos/sustentabilidade/plano-abc/arquivo-publicacoes-plano-abc/download.pdf
Braun C, Zumft WG (1991) Marker exchange of the structural genes for nitric oxide reductase blocks the denitrification pathway of Pseudomonas stutzeri at nitric oxide. J Biol Chem 266:22785–22788
Breitenbeck GA, Bremner JM (1989) ability of free-living cells of Bradyrhizobium japonicum to denitrify in soils. Biol Fertil Soils 7:219–224. https://doi.org/10.1007/bf00709652
Bueno E, Robles EF, Torres MJ, Krell T, Bedmar EJ, Delgado MJ, Mesa S (2017) Disparate response to microoxia and nitrogen oxides of the Bradyrhizobium japonicum napEDABC, nirK and norCBQD denitrification genes. Nitric Oxide 68:137–149. https://doi.org/10.1016/j.niox.2017.02.002
Casella S, Leporini C, Nuti MP (1984) Nitrous oxide production by nitrogen-fixing, fast-growing rhizobia. Microb Ecol 10:107–114. https://doi.org/10.1007/bf02011418
Chalk PM (1997) Dynamics of biologically fixed N in legume-cereal rotations: a review. Aust J Agric Res 49:303–316. https://doi.org/10.1071/A97013
Chen H, Li X, Hu F, Shi W (2013) Soil nitrous oxide emissions following crop residue addition: a meta-analysis. Glob Chang Biol 19:2956–2964. https://doi.org/10.1111/gcb.12274
Ciais P et al (2014) Carbon and other biogeochemical cycles. In: 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, pp 465–570
Ciampitti IA, Ciarlo EA, Conti ME (2008) Nitrous oxide emissions from soil during soybean [(Glycine max (L.) Merrill] crop phenological stages and stubbles decomposition period Biol Fertil Soils 44:581-588 https://doi.org/10.1007/s00374-007-0241-7
Cohen MF, Lamattina L, Yamasaki H (2009) Nitric oxide signaling by plant-associated Bacteria. In: Hayat S, Mori M, Pichtel J, Ahmad A (eds) Nitric oxide in plant physiology. Wiley-Blackwell, Chichester, pp 161–172. https://doi.org/10.1002/9783527629138.ch11
Corpas F, Barroso J (2015) Functions of nitric oxide (NO) in roots during development and under adverse stress conditions. Plants 4:240–252
Coyotzi S, Doxey AC, Clark ID, Lapen DR, Van Cappellen P, Neufeld JD (2017) Agricultural soil denitrifiers possess extensive nitrite reductase gene diversity. Environ Microbiol 19:1189–1208. https://doi.org/10.1111/1462-2920.13643
Daims H, Nielsen JL, Nielsen PH, Schleifer K-H, Wagner M (2001) In Situ characterization of Nitrospira-like nitrite-oxidizing Bacteria active in wastewater treatment plants. Appl Environ Microbiol 67:5273–5284. https://doi.org/10.1128/aem.67.11.5273-5284.2001
Damiani I, Pauly N, Puppo A, Brouquisse R, Boscari A (2016) Reactive oxygen species and nitric oxide control early steps of the legume – Rhizobium symbiotic interaction. Front Plant Sci 7:1–8. https://doi.org/10.3389/fpls.2016.00454
Danneberg G, Kronenberg A, Neuer G, Bothe H (1986) Aspects of nitrogen fixation and denitrification by Azospirillum. Plant Soil 90:193–202. https://doi.org/10.1007/bf02277396
Davidson EA, Verchot LV (2000) Testing the hole-in-the-pipe model of nitric and nitrous oxide emissions from soils using the TRAGNET database. Glob Biogeochem Cycles 14:1035–1043. https://doi.org/10.1029/1999gb001223
de Freitas PL, Landers JN (2014) The transformation of agriculture in Brazil through development and adoption of zero tillage conservation agriculture. International Soil and Water Conservation Research (ISWCR) 2:35–34. https://doi.org/10.1016/S2095-6339(15)30012-5
Delamuta JRM, Ribeiro RA, Ormeño-Orrillo E, Melo IS, Martínez Romero E, Hungria M (2013) Polyphasic evidence supporting the reclassification of Bradyrhizobium japonicum group Ia strains as Bradyrhizobium diazoefficiens sp. nov. Int J Syst Evol Microbiol 63:3342–3351. https://doi.org/10.1099/ijs.0.049130-0
Delgado MJ, Casella S, Bedmar EJ (2007) Denitrification in rhizobia-legume symbiosis. In: Bothe H, Ferguson SJ, Newton WE (eds) Biology of the nitrogen cycle. Elservier Science, Amsterdam, pp 57–66. https://doi.org/10.1016/B978-044452857-5.50007-2
Dobereiner J, Pedrosa FO (1987) Nitrogen-fixing bacteria in nonleguminous crop plants. Science Tech Publishers
Dong Z, Layzell DB (2001) H2 oxidation, O2 uptake and CO2 fixation in hydrogen treated soils. Plant Soil 229:1–12. https://doi.org/10.1023/a:1004810017490
Flynn B, Graham A, Scott N, Layzell DB, Dong Z (2014) Nitrogen fixation, hydrogen production and N2O emissions. Can J Plant Sci 94:1037–1041. https://doi.org/10.1139/cjps2013-210
Fowler, D. et al., (2013). The global nitrogen cycle in the 21st century. Phil Trans Roy Soc Lond Ser B 368: 20130164. 2013. https://doi.org/10.1098/rstb.2013.0164
Fujikake H et al (2003) quick and reversible inhibition of soybean root nodule growth by nitrate involves a decrease in sucrose supply to nodules. J Exp Bot 54:1379–1388. https://doi.org/10.1098/rstb.2013.0164
Gallegos MT, Schleif R, Bairoch A, Hofmann K, Ramos JL (1997) Arac/XylS family of transcriptional regulators. Microbiol Mol Biol Rev 61:393–410
Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892. https://doi.org/10.1126/science.1136674
Garcia-Plazaola JI, Becerril JM, Arrese-Igor C, Hernandez A, Gonzalez-Murua C, Aparicio-Tejo PM (1993) Denitrifying ability of thirteen Rhizobium meliloti strains. Plant Soil 149:43–50. https://doi.org/10.1007/bf00010761
Hénault C, Revellin C (2011) Inoculants of leguminous crops for mitigating soil emissions of the greenhouse gas nitrous oxide. Plant Soil 346:289–296. https://doi.org/10.1007/s11104-011-0820-0
Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311:1–18. https://doi.org/10.1007/s11104-008-9668-3
Hungria M, Mendes IC (2015) Nitrogen fixation with soybean: the perfect symbiosis? In: de Bruijn FJ (ed) Biological nitrogen fixation. John Wiley & Sons, Inc, New Jersey, pp 1009–1024. https://doi.org/10.1002/9781119053095.ch99
Inaba S, Tanabe K, Eda S, Ikeda S, Higashitani A, Mitsui H, Minamisawa K (2009) Nitrous oxide emission and microbial community in the rhizosphere of nodulated soybeans during the late growth period. Microbes Environ 24:64–67. https://doi.org/10.1264/jsme2.ME08544
Inaba S, Ikenishi F, Itakura M, Kikuchi M, Eda S, Chiba N, Katsuyama C, Suwa Y, Mitsui H, Minamisawa K (2012) N2O emission from degraded soybean nodules depends on denitrification by Bradyrhizobium japonicum and other microbes in the rhizosphere. Microbes Environ 27:470–476. https://doi.org/10.1264/jsme2.ME12100
Itakura M, Tabata K, Eda S, Mitsui H, Murakami K, Yasuda J, Minamisawa K (2008) Generation of Bradyrhizobium japonicum mutants with increased N2O reductase activity by selection after introduction of a mutated dnaQ gene. Appl Environ Microbiol 74:7258–7264. https://doi.org/10.1128/aem.01850-08
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 nature. Clim Chang 3:208–212. https://doi.org/10.1038/NCLIMATE1734
Jensen ES, Peoples MB, Boddey RM, Gresshoff PM, Hauggaard-Nielsen H, J.R. Alves B, Morrison MJ (2012) Legumes for mitigation of climate change and the provision of feedstock for biofuels and biorefineries. A review Agron Sustain Dev 32:329–364. https://doi.org/10.1007/s13593-011-0056-7
Jones CM, Stres B, Rosenquist M, Hallin S (2008) Phylogenetic Analysis of Nitrite, Nitric Oxide, and Nitrous Oxide Respiratory Enzymes Reveal a Complex Evolutionary History for Denitrification Molecular Biology and Evolution 25:1955–1966 doi: https://doi.org/10.1093/molbev/msn146
Jørgensen RN, JØrgensen BJ, Nielsen NE (1998) N 2 O emission immediately after rainfall in a dry stubble field. Soil Biol Biochem 30:545–546
Kirchman DL (2011) Processes in microbial ecology. Oxford University Press, Oxford. https://doi.org/10.1093/acprof:oso/9780199586936.001.0001
Kloos K, Mergel A, Rösch C, Bothe H (2001) Denitrification within the genus Azospirillum and other associative bacteria. Funct Plant Biol 28:991–998. https://doi.org/10.1071/PP01071
Kondorosi E, Mergaert P, Kereszt A (2013) A paradigm for endosymbiotic life: cell differentiation of rhizobium Bacteria provoked by host plant factors. Annu Rev Microbiol 67:611–628. https://doi.org/10.1146/annurev-micro-092412-155630
Kool DM, Dolfing J, Wrage N, Van Groenigen JW (2011) Nitrifier denitrification as a distinct and significant source of nitrous oxide from soil. Soil Biol Biochem 43:174–178. https://doi.org/10.1016/j.soilbio.2010.09.030
Kraft B, Strous M, Tegetmeyer HE (2011) Microbial nitrate respiration –g, enzymes and environmental distribution. J Biotechnol 155:104–117. https://doi.org/10.1016/j.jbiotec.2010.12.025
Laughlin RJ, Rütting T, Müller C, Watson CJ, Stevens RJ (2009) Effect of acetate on soil respiration, N2O emissions and gross N transformations related to fungi and bacteria in a grassland soil. Appl Soil Ecol 42:25–30. https://doi.org/10.1016/j.apsoil.2009.01.004
Layzell DB, Hunt S (1990) Oxygen and the regulation of nitrogen fixation in legume nodules. Physiol Plant 80:322–327. https://doi.org/10.1111/j.1399-3054.1990.tb04414.x
Leach J, Keyster M, Du Plessis M, Ludidi N (2010) Nitric oxide synthase activity is required for development of functional nodules in soybean. J Plant Physiol 167:1584–1591. https://doi.org/10.1016/j.jplph.2010.06.019
Lecomte SM, Achouak W, Abrouk D, Heulin T, Nesme X, Haichar FeZ (2018) Diversifying anaerobic respiration strategies to compete in the rhizosphere. Frontiers in Environmental Science 6. https://doi.org/10.3389/fenvs.2018.00139
Li X, Hu F, Shi W (2013) Plant material addition affects soil nitrous oxide production differently between aerobic and oxygen-limited conditions. Appl Soil Ecol 64:91–98. https://doi.org/10.1016/j.apsoil.2012.10.003
Maeda K, Spor A, Edel-Hermann V, Heraud C, Breuil MC, Bizouard F, Toyoda S, Yoshida N, Steinberg C, Philippot L (2015) N2O production, a widespread trait in fungi. Sci Rep 5:9697. https://doi.org/10.1038/srep09697
Marusenko Y, Huber DP, Hall SJ (2013) Fungi mediate nitrous oxide production but not ammonia oxidation in aridland soils of the southwestern US. Soil Biol Biochem 63:24–36. https://doi.org/10.1016/j.soilbio.2013.03.018
Mathieu C, Moreau S, Frendo P, Puppo A, Davies MJ (1998) Direct detection of radicals in intact soybean nodules: presence of nitric oxide-leghemoglobin complexes free radical. Biol Med 24:1242–1249. https://doi.org/10.1016/S0891-5849(97)00440-1
Mavromatis K, Ivanova NN, Chen IMA, Szeto E, Markowitz VM, Kyrpides NC (2009) The DOE-JGI standard operating procedure for the annotations of microbial genomes. Stand Genomic Sci 1:63–67. https://doi.org/10.4056/sigs.632
Meakin GE, Bueno E, Jepson B, Bedmar EJ, Richardson DJ, Delgado MJ (2007) The contribution of bacteroidal nitrate and nitrite reduction to the formation of nitrosylleghaemoglobin complexes in soybean root nodules. Microbiology 153:411–419. https://doi.org/10.1099/mic.0.2006/000059-0
Mesa S, Alché JD, Bedmar E, Delgado MJ (2004) Expression of nir, nor and nos denitrification genes from Bradyrhizobium japonicum in soybean root nodules. Physiol Plant 120:205–211. https://doi.org/10.1111/j.0031-9317.2004.0211.x
Minchin FR (1997) Regulation of oxygen diffusion in legume nodules. Soil Biol Biochem 29:881–888. https://doi.org/10.1016/S0038-0717(96)00204-0
Molina-Henares AJ, Krell T, Eugenia Guazzaroni M, Segura A, Ramos JL (2006) Members of the IclR family of bacterial transcriptional regulators function as activators and/or repressors. FEMS Microbiol Rev 30:157–186. https://doi.org/10.1111/j.1574-6976.2005.00008.x
Monteiro, RC (2016) Emissões de N2O em diferentes sucessões de cultura em dois sistemas de preparo do solo para produção de soja. MSc. Thesis. Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ, Brazil
Morais, RF (2012) Manejo da adubação nitrogenada e emissão de gases de efeito estufa em capim-elefante para bioenergia.PhD. Thesis. Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ, Brazil
Nascimento, EC (2011) Potencial desnitrificador de estirpes de Bradyrhizobium recomendadas para a cultura da soja. MSc. Thesis. Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ, Brazil
Nelson LM, Knowles R (1978) Effect of oxygen and nitrate on nitrogen fixation and denitrification by Azospirillum brasilense grown in continuous culture. Can J Microbiol 24:1395–1403. https://doi.org/10.1139/m78-223
Nömmik H (1956) Investigations on denitrification in Soil. Acta Agriculturae Scandinavica 6:195–228 https://doi.org/10.1080/00015125609433269
O’Hara GW, Daniel RM, Steele KW, Bonish PM (1984) Nitrogen losses from soils caused by Rhizobium-dependent denitrification. Soil Biol Biochem 16:429–431. https://doi.org/10.1016/0038-0717(84)90047-6
Obando M, Correa-Galeote D, Castellano-Hinojosa A, Gualpa J, Hidalgo A, Alché JD, Bedmar E, Cassán F (2019) Analysis of the denitrification pathway and greenhouse gases emissions in Bradyrhizobium sp. strains used as biofertilizers in South America. J Appl Microbiol. https://doi.org/10.1111/jam.14233
Odu CTI, Adeoye KB (1970) Heterotrophic nitrification in soils— a preliminary investigation. Soil Biol Biochem 2:41–45. https://doi.org/10.1016/0038-0717(70)90024-6
O'Hara GW, Daniel RM (1985) Rhizobial denitrification: A review. Soil Biol Biochem 17:1–9. https://doi.org/10.1016/0038-0717(85)90082-3
O'Hara GW, Daniel RM, Steele KW (1983) Effect of oxygen on the synthesis, activity and breakdown of the Rhizobium denitrification system. Microbiology 129:2405–2412. https://doi.org/10.1099/00221287-129-8-2405
Oono R, Denison RF (2010) Comparing symbiotic efficiency between swollen versus nonswollen rhizobial bacteroids. Plant Physiol 154:1541–1548. https://doi.org/10.1104/pp.110.163436
Overbeek R, Fonstein M, D’Souza M, Pusch GD, Maltsev N (1999) The use of gene clusters to infer functional coupling. Proc Natl Acad Sci 96:2896–2901. https://doi.org/10.1073/pnas.96.6.2896
Parker CA, Trinick MJ, Chatel DL (1976) Rhizobia as soil rhizosphere inhabitants. In: Hardy RW (ed) A treatise on Dinitrogen Fixation. John Wiley & Son, New York, pp 311–352 200
Parkin TB (1987) Soil microsites as a source of denitrification variability 1. Soil Sci Soc Am J 51:1194–1199. https://doi.org/10.2136/sssaj1987.03615995005100050019x
Petrova LP, Varshalomidze OE, Shelud’ko AV, Katsy EI (2010) Localization of denitrification genes in plasmid DNA of bacteria Azospirillum brasilense. Russ J Genet 4:801–807
Pett-Ridge J, Silver WL, Firestone MK (2006) Redox fluctuations frame microbial community impacts on N-cycling rates in a humid tropical forest soil. Biogeochemistry 81:95–110. https://doi.org/10.1007/s10533-006-9032-8
Philippot L (2002) Denitrifying genes in bacterial and archaeal genomes. Biochim Biophys Acta (BBA) 1577:355–376. https://doi.org/10.1016/S0167-4781(02)00420-7
Philippot L, Hallin S, Schloter M (2007) Ecology of denitrifying prokaryotes in agricultural soil. In: advances in agronomy, vol 96. Academic press, pp 249–305. https://doi.org/10.1016/S0065-2113(07)96003-4
Pothier JF, Prigent-Combaret C, Haurat J, Moenne-Loccoz Y, Wisniewski-Dye F (2008) Duplication of plasmid-borne nitrite reductase gene nirK in the wheat-associated plant growth–promoting rhizobacterium Azospirillum brasilense Sp245. Mol Plant Microbe Interact 21:831–842. https://doi.org/10.1094/MPMI-21-6-0831
Rivera D, Revale S, Molina R, Gualpa J, Puente M, Maroniche G, Paris G, Baker D, Clavijo B, McLay K, Spaepen S, Perticari A, Vazquez M, Wisniewski-Dye F, Watkins C, Martinez-Abarca F, Vanderleyden J, Cassan F (2014) Complete genome sequence of the model rhizosphere strain Azospirillum brasilense Az39, successfully applied in agriculture. Genome Announcement 2:e00683–e00614. https://doi.org/10.1128/genomeA.00683-14
Robertson GP, Grace PR (2004) Greenhouse gas fluxes in tropical and temperate agriculture: the need for a full-cost accounting of global warming potentials. Environ Dev Sustain 6:51–63. https://doi.org/10.1023/B:ENVI.0000003629.32997.9e
Robertson GP, Groffman PM (2007) 13 - nitrogen transformations A2 - PAUL, ELDOR a. In: Soil microbiology, ecology and biochemistry, Third edn. Academic Press, San Diego, pp 341–364. https://doi.org/10.1016/B978-0-08-047514-1.50017-2
Rochette P (2008) No-till only increases N2O emissions in poorly-aerated soils. Soil Tillage Res 101:97–100. https://doi.org/10.1016/j.still.2008.07.011
Rochette P, Janzen HH (2005) Towards a revised coefficient for estimating N2O emissions from legumes. Nutr Cycl Agroecosyst 73:171–179. https://doi.org/10.1007/s10705-005-0357-9
Saito A et al (2014) Effect of nitrate on nodule and root growth of soybean (Glycine max (L.) Merr.). Int J Mol Sci 15:4464–4480. https://doi.org/10.3390/ijms15034464
Sameshima-Saito R, Chiba K, Minamisawa K (2006) Correlation of denitrifying capability with the existence of nap, nir, nor and nos genes in diverse strains of soybean Bradyrhizobia. Microbes Environ 21:174–184. https://doi.org/10.1264/jsme2.21.174
Sánchez C, Cabrera Juan J, Gates Andrew J, Bedmar Eulogio J, Richardson David J, Delgado María J (2011) Nitric oxide detoxification in the rhizobia–legume symbiosis. Biochem Soc Trans 39:184–188. https://doi.org/10.1042/bst0390184
Schubert KR, Evans HJ (1976) Hydrogen evolution: a major factor affecting the efficiency of nitrogen fixation in nodulated symbionts. Proc Natl Acad Sci 73:1207–1211
Schwab S, Terra LA, Baldani JI (2018) Genomic characterization of Nitrospirillum amazonense strain CBAmC, a nitrogen-fixing bacterium isolated from surface-sterilized sugarcane stems. Mol Gen Genomics 293:997–1016. https://doi.org/10.1007/s00438-018-1439-0
Shiina Y, Itakura M, Choi H, Saeki Y, Hayatsu M, Minamisawa K (2014) Relationship between soil type and N2O reductase genotype (nosZ) of indigenous soybean bradyrhizobia: nosZ-minus populations are dominant in andosols. Microbes Environ 29:420–426. https://doi.org/10.1264/jsme2.ME14130
Shimizu T, Nakamura A (2014) Characterization of LgnR, an IclR family transcriptional regulator involved in the regulation of l-gluconate catabolic genes in Paracoccus sp. 43P. Microbiology 160:623–634. https://doi.org/10.1099/mic.0.074286-0
Shoun H, Fushinobu S, Jiang L, Kim S-W, Wakagi T (2012) Fungal denitrification and nitric oxide reductase cytochrome P450nor. Philos Trans R Soc, B 367:1186–1194. https://doi.org/10.1098/rstb.2011.0335
Smith GB, Smith MS (1986) Symbiotic and free-living denitrification by Bradyrhizobium japonicum 1. Soil Sci Soc Am J 50:349–354. https://doi.org/10.2136/sssaj1986.03615995005000020019x
Smith MS, Tiedje JM (1979) Phases of denitrification following oxygen depletion in soil soil. Biol Biochem 11:261–267. https://doi.org/10.1016/0038-0717(79)90071-3
Smith KA, Ball T, Conen F, Dobbie KE, Massheder J, Rey A (2003) Exchange of greenhouse gases between soil and atmosphere: interactions of soil physical factors and biological processes. Eur J Soil Sci 54:779–791. https://doi.org/10.1046/j.1351-0754.2003.0567.x
Sparacino-Watkins C, Stolz JF, Basu P (2014) Nitrate and periplasmic nitrate reductases. Chem Soc Rev 43:676–706. https://doi.org/10.1039/c3cs60249d
Stange CF, Spott O, Arriaga H, Menéndez S, Estavillo JM, Merino P (2013) Use of the inverse abundance approach to identify the sources of NO and N2O release from Spanish forest soils under oxic and hypoxic conditions. Soil Biol Biochem 57:451–458. https://doi.org/10.1016/j.soilbio.2012.10.006
Steenhoudt O, Keijers V, Okon Y, et al. Arch Microbiol (2001) 175:344. https://doi.org/10.1007/s002030100271
Strohm TO, Griffin B, Zumft WG, Schink B (2007) Growth yields in bacterial denitrification and nitrate ammonification. Appl Environ Microbiol 73:1420–1424. https://doi.org/10.1128/aem.02508-06
Sugawara M, Sadowsky MJ (2013) Influence of elevated atmospheric carbon dioxide on transcriptional responses of Bradyrhizobium japonicum in the soybean rhizoplane. Microbes Environ 28:217–227. https://doi.org/10.1264/jsme2.ME12190
Torres María J, Bueno E, Mesa S, Bedmar Eulogio J, Delgado María J (2011) Emerging complexity in the denitrification regulatory network of Bradyrhizobium japonicum. Biochem Soc Trans 39:284–288. https://doi.org/10.1042/bst0390284
Tortosa G, Hidalgo A, Salas A, Bedmar EJ, Mesa S, Delgado MJ (2015) Nitrate and flooding induce N2O emissions from soybean nodules. Symbiosis 67:125–133. https://doi.org/10.1007/s13199-015-0341-3
Uchida Y, Akiyama H (2013) Mitigation of postharvest nitrous oxide emissions from soybean ecosystems: a review. Soil Sci Plant Nutr 59:477–487. https://doi.org/10.1080/00380768.2013.805433
van Spanning RJM, Richardson DJ, Ferguson SJ (2007) Introduction to the biochemistry and molecular biology of denitrification. In: Bothe H, Ferguson SJ, Newton WE (eds) Biology of the nitrogen cycle. Part I: denitrification. Elsevier, Amsterdam, pp 3–20. https://doi.org/10.1016/B978-044452857-5.50002-3
Wang Y, Uchida Y, Shimomura Y, Akiyama H, Hayatsu M, (2017) Responses of denitrifying bacterial communities to short–term waterlogging of soils. Scientific Reports 7 (1). https://doi.org/10.1038/s41598-017-00953-8
Viera-Vargas MS, Souto CM, Urquiaga S, Boddey RM (1995) Quantification of the contribution of N2 fixation to tropical forage legumes and transfer to associated grass. Soil Biol Biochem 27:1193–1200. https://doi.org/10.1016/0038-0717(95)00022-7
World Meteorological Organization (2014) WMO statement on the status of the global climate in 2013. Switzerland, Geneva
Yang L, Cai Z (2005) The effect of growing soybean (Glycine max. L.) on N2O emission from soil. Soil Biol Biochem 37:1205–1209. https://doi.org/10.1016/j.soilbio.2004.08.027
Zablotowicz RM, Focht DD (1979) Denitrification and anaerobic, nitrate-dependent acetylene reduction in cowpea Rhizobium. Microbiology 111:445–448
Zablotowicz RM, Eskew DL, Focht DD (1978) Denitrification in Rhizobium. Can J Microbiol 24:757–760. https://doi.org/10.1139/m78-126
Zhang J, Zhu T, Cai Z, Müller C (2011) Nitrogen cycling in forest soils across climate gradients in eastern China. Plant Soil 342:419–432. https://doi.org/10.1007/s11104-010-0706-6
Zhong Z, Lemke RL, Nelson LM (2009) Nitrous oxide emissions associated with nitrogen fixation by grain legumes. Soil Biol Biochem 41:2283–2291
Zhu T, Meng T, Zhang J, Zhong W, Müller C, Cai Z (2015) Fungi-dominant heterotrophic nitrification in a subtropical forest soil of China. J Soils Sediments 15:705–709. https://doi.org/10.1007/s11368-014-1048-4
Zilli JE, Pereira GMD, França Júnior I, Kd S, Hungria M, Rouws JRC (2013) Dynamic of rhizobia in the soil during the dry season in cerrado of Roraima. Acta Amazon 43:153–160
Zotarelli L, Zatorre NP, Boddey RM, Urquiaga S, Jantalia CP, Franchini JC, Alves BJR (2012) Influence of no-tillage and frequency of a green manure legume in crop rotations for balancing N outputs and preserving soil organic C stocks. Field Crop Res 132:185–195. https://doi.org/10.1016/j.fcr.2011.12.013
Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:533–616
Acknowledgments
We thank Dr. Robert M. Boddey for reviewing the manuscript and providing helpful suggestions. We also thank the CNPq (Brazilian National Council for Scientific and Technological Development), FONCyT and CONICET (Argentina) for productivity grants awarded to some of the authors and financial support of projects, especially INCT Plant Growth–Promoting Microorganisms for Agricultural Sustainability and Environmental Responsibility (465133/2014-2).
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Zilli, J.É., Alves, B.J.R., Rouws, L.F.M. et al. The importance of denitrification performed by nitrogen-fixing bacteria used as inoculants in South America. Plant Soil 451, 5–24 (2020). https://doi.org/10.1007/s11104-019-04187-7
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DOI: https://doi.org/10.1007/s11104-019-04187-7