Rhizobium etli is able to emit nitrous oxide by connecting assimilatory nitrate reduction with nitrite respiration in the bacteroids of common bean nodules

References

• Berger A, Boscari A, Frendo P, Brouquisse R. 2019. Nitric oxide signaling, metabolism and toxicity in nitrogen-fixing symbiosis. J Exp Bot. 70:4505–4520. doi:10.1093/jxb/erz159.
   PubMed Web of Science ®Google Scholar
• Beringer JE. 1974. R factor transfer in Rhizobium leguminosarum. J Gen Microbiol. 84:188–198.
   PubMedGoogle Scholar
• Blanquet P, Silva L, Catrice O, Bruand C, Carvalho H, Meilhoc E. 2015. Sinorhizobium meliloti controls nitric oxide–mediated post-translational modification of a Medicago truncatula nodule protein. Mol Plant-Microbe Interact. 28:1353–1363. doi:10.1094/MPMI-05-15-0118-R.
   PubMed Web of Science ®Google Scholar
• Bravo A, Mora J. 1988. Ammonium assimilation in Rhizobium phaseoli by the glutamine synthetase-glutamate synthase pathway. J Bacteriol. 170:980–984. doi:10.1128/jb.170.2.980-984.1988.
   PubMed Web of Science ®Google Scholar
• 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, B Biol Sci. 368:1–13. doi:10.1098/rstb.2013.0122.
   Web of Science ®Google Scholar
• Cabrera JJ, Salas A, Torres MJ, Bedmar EJ, Richardson DJ, Gates AJ, Delgado MJ. 2016. An integrated biochemical system for nitrate assimilation and nitric oxide detoxification in Bradyrhizobium japonicum. Biochem J. 473:297–309. doi:10.1042/BJ20150880.
   PubMed Web of Science ®Google Scholar
• Calvo-Begueria L, Rubio MC, Martínez JI, Pérez-Rontomé C, Delgado MJ, Bedmar EJ, Becana M. 2018. Redefining nitric oxide production in legume nodules through complementary insights from electron paramagnetic resonance spectroscopy and specific fluorescent probes. J Exp Bot. 69:3703–3714. doi:10.1093/jxb/ery159.
   PubMed Web of Science ®Google Scholar
• Delgado MJ, Bonnard N, Tresierra-Ayala A, Bedmar EJ, Muller P. 2003. The Bradyrhizobium japonicum napEDABC genes encoding the periplasmic nitrate reductase are essential for nitrate respiration. Microbiology. 149:3395–3403. doi:10.1099/mic.0.26620-0.
   PubMed Web of Science ®Google Scholar
• Delgado MJ, Casella S, Bedmar EJ. 2007. Denitrification in rhizobia-legume symbiosis. In: Bothe H, Ferguson SJ, Newton WE, editor. Biology of the nitrogen cycle. Amsterdam: Elsevier Science; p. 57–66.
   Google Scholar
• Delgado MJ, Ligero F, Lluch C. 1994. Effect of salt stress on growth and nitrogen fixation by pea, faba bean, common bean and soybean plants. Soil Biol Biochem. 26:371–376. doi:10.1016/0038-0717(94)90286-0.
   Web of Science ®Google Scholar
• Gates AJ, Luque-Almagro VM, Goddard AD, Ferguson SJ, Roldan MD, Richardson DJ. 2011. A composite biochemical system for bacterial nitrate and nitrite assimilation as exemplified by Paracoccus denitrificans. Biochem J. 435:743–753. doi:10.1042/BJ20101920.
   PubMed Web of Science ®Google Scholar
• Goddard AD, Bali S, Mavridou DA, Luque-Almagro VM, Gates AJ, Roldán MD, Newstead S, Richardson DJ, Ferguson SJ. 2017. The Paracoccus denitrificans NarK-like nitrate and nitrite transporters probing nitrate uptake and nitrate/nitrite exchange mechanisms. Mol Microbiol. 103:117–133. doi:10.1111/mmi.13546.
   PubMed Web of Science ®Google Scholar
• Goddard AD, Moir JW, Richardson DJ, Ferguson SJ. 2008. Interdependence of two NarK domains in a fused nitrate/nitrite transporter. Mol Microbiol. 70:667–681. doi:10.1111/j.1365-2958.2008.06436.x.
   PubMed Web of Science ®Google Scholar
• Gómez-Hernández N, Reyes-González A, Sánchez C, Mora Y, Delgado MJ, Girard L. 2011. Regulation and symbiotic role of nirK and norC expression in Rhizobium etli. Mol Plant-Microbe Interact. 24:233–245. doi:10.1094/MPMI-07-10-0173.
   PubMed Web of Science ®Google Scholar
• Graham PH, Vance CP. 2003. Legume Importance and Constraints to Greater Use. Plant Physiol. 131:872–877. doi:10.1104/pp.017004.
   PubMed Web of Science ®Google Scholar
• Hein S, Simon J. 2019. Bacterial nitrous oxide respiration: electron transport chains and copper transfer reactions. Adv Microb Physiol. 75:137–175. doi:10.1016/bs.ampbs.2019.07.001.
   PubMed Web of Science ®Google Scholar
• Hidalgo-García A, Torres MJ, Salas A, Bedmar EJ, Girard L, Delgado MJ. 2019. Rhizobium etli produces nitrous oxide by coupling the assimilatory and denitrification pathways. Front Microbiol. 10:1–11. doi:10.3389/fmicb.2019.00980.
   PubMed Web of Science ®Google Scholar
• Hidalgo-García A, Tortosa G, Bedmar EJ, Delgado MJ. 2016. Efecto del nitrato y el encharcamiento en la emisión del gas invernadero N2O por la simbiosis Phaseolus vulgaris-Rhizobium etli. In: Clemente A, De Ron AM, editors. 7ª acta de la asociación española de leguminosas. Granada: Editorial Atrio S.L.; p. 51–61.
   Google Scholar
• Hirayama J, Eda S, Mitsui H, Minamisawa K. 2011. Nitrate dependent N2O emission from intact soybean nodules via denitrification by Bradyrhizobium japonicum bacteroids. Appl Environ Microbiol. 77:8787–8790. doi:10.1128/AEM.06262-11.
   PubMed Web of Science ®Google Scholar
• Horchani F, Prévot M, Boscari A, Evangelisti E, Meilhoc E, Bruand C, Raymond P, Boncompagni E, Aschi-Smiti S, Puppo A, Brouquisse R. 2010. Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatula nitrogen-fixing nodules. Plant Physiol. 155:1023–1036. doi:10.1104/pp.110.166140.
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1264/jsme2.ME12100.
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1264/jsme2.ME08544.
   PubMed Web of Science ®Google Scholar
• IPCC. 2019. Summary for policymakers. In: Shukla PR, Skea J, Calvo Buendía E, Masson-Delmotte V, Pörtner H-O, Roberts DC, Zhai P, Slade R, Connors S, van Diemen R., et al., editors. Climate change and land: An IPCC special report on climate change, desertification, land degradation, sustainable land management, food security, and greenhouse Gas fluxes in terrestrial ecosystems. Geneva: Intergovernmental panel on climate change; p. 1–34.
   Google Scholar
• Kovach ME, Phillips RW, Elzer PH, Roop RM, Peterson KM. 1994. pBBR1MCS: a broad-host-range cloning vector. Biotechniques. 16:800–802.
   PubMed Web of Science ®Google Scholar
• Kudeyarov VN. 2020. Nitrous oxide emission from fertilized soils: an analytical review. Eurasian Soil Science. 53(10):1396–1407. doi:10.1134/S1064229320100105.
   Web of Science ®Google Scholar
• LaRue TA, Child JJ. 1979. Sensitive fluorometric assay for leghemoglobin. Anal Biochem. 92:11–15. doi:10.1016/0003-2697(79)90618-3.
   PubMed Web of Science ®Google Scholar
• Lazcano C, Zhu-Barker X, Decock C. 2021. Effects of organic fertilizers on the soil microorganisms responsible for N2O emissions: a review. Microorganisms. 9:983. doi:10.3390/microorganisms9050983.
   PubMed Web of Science ®Google Scholar
• Luque-Almagro VM, Lyall VJ, Ferguson SJ, Roldan MD, Richardson DJ, Gates AJ. 2013. Nitrogen oxyanion-dependent dissociation of a two-component complex that regulates bacterial nitrate assimilation. J Biol Chem. 288:29692–29702. doi:10.1074/jbc.M113.459032.
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1099/mic.0.2006/000059-0.
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1111/j.0031-9317.2004.0211.x.
   PubMed Web of Science ®Google Scholar
• Moir JW, Wood NJ. 2001. Nitrate and nitrite transport in bacteria. Cell Mol Life Sci. 58:215–224. doi:10.1007/PL00000849.
   PubMed Web of Science ®Google Scholar
• Müller R. 2021. The impact of the rise in atmospheric nitrous oxide on stratospheric ozone. Ambio. 50:35–39. doi:10.1007/s13280-020-01428-3.
   PubMed Web of Science ®Google Scholar
• Nicholas DJ, Nason A. 1957. Determination of nitrate and nitrite. Meth Enzymol. 3:981–984. doi:10.1016/S0076-6879(57)03489-8.
   Web of Science ®Google Scholar
• Noel K D, Sanchez A, Fernandez L, Leemans J, Cevallos M A. 1984. Rhizobium phaseoli symbiotic mutants with transposon Tn5 insertions. Journal of Bacteriology. 158(1):148–155. http://doi.org/10.1128/jb.158.1.148-155.1984.
   PubMed Web of Science ®Google Scholar
• Pilegaard K. 2013. Processes regulating nitric oxide emissions from soils. Philos Trans R Soc Lond B Biol Sci. 368(1621):20130126. doi:10.1098/rstb.2013.0126.
   PubMed Web of Science ®Google Scholar
• Rigaud J, Puppo A. 1975. Indole-3-acetic acid catabolism by soybean bacteroids. J Gen Microbiol. 88:223–228. doi:10.1099/00221287-88-2-223.
   Google Scholar
• Ruiz B, Sauviac L, Brouquisse R, Bruand C, Meilhoc E. 2022. Role of nitric oxide of bacterial origin in the Medicago truncatula-Sinorhizobium meliloti symbiosis. Mol Plant Microbe Interact. 35:887–892. doi:10.1094/MPMI-05-22-0118-SC.
   PubMed Web of Science ®Google Scholar
• Salas A, Cabrera JJ, Jiménez-Leiva A, Mesa S, Bedmar EJ, Richardson DJ, Gates AJ, Delgado MJ. 2021. Bacterial nitric oxide metabolism: recent insights in rhizobia. Adv Microb Physiol. 78:259–315. doi:10.1016/bs.ampbs.2021.05.001.
   PubMed Web of Science ®Google Scholar
• Salas A, Tortosa G, Hidalgo-García A, Delgado A, Bedmar EJ, Richardson DJ, Gates AJ, Delgado MJ. 2020. The Hemoglobin Bjgb from Bradyrhizobium diazoefficiens controls NO homeostasis in soybean nodules to protect symbiotic nitrogen fixation. Front Microbiol. 10:2915. doi:10.3389/fmicb.2019.02915.
   PubMed Web of Science ®Google Scholar
• Sambrook J, Fritsch EF, Maniatics T. 1989. Molecular cloning: A laboratory manual. New York: Cold Spring Harbor Laboratory, Cold Spring Harbor.
   Google Scholar
• Sambrook J, Russell D. 2001. Molecular cloning: a laboratory manual, 3rd ed. New York: Cold Spring Harbor Laboratory, Cold Spring Harbor.
   Google Scholar
• Sánchez C, Gates AJ, Meakin GE, Uchiumi T, Girard L, Richardson DJ, Bedmar EJ, Delgado MJ. 2010. Production of nitric oxide and nitrosylleghaemoglobin complexes in soybean nodules in response to flooding. Mol Plant Microbe Interact. 23:702–711. doi:10.1094/MPMI-23-5-0702.
   PubMed Web of Science ®Google Scholar
• Sánchez C, Minamisawa K. 2019. Nitrogen cycling in soybean rhizosphere: sources and sinks of nitrous oxide (N2O). Front Microbiol. 10(1943):1–7. doi:10.3389/fmicb.2019.01943.
   PubMedGoogle Scholar
• Schäfer A, Tauch A, Jäger W, Kalinowski J, Thierbach G, Pühler A. 1994. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene. 145:69–73. doi:10.1016/0378-1119(94)90324-7.
   PubMed Web of Science ®Google Scholar
• Simon R, Priefer U, Pühler A. 1983. Molecular Genetics of the Bacteria-Plant Interaction. Heidelberg: Springer.
   Google Scholar
• Thomson AJ, Giannopulos 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, B Biol Sci. 367:1157–1168. doi:10.1098/rstb.2011.0415.
   PubMed Web of Science ®Google Scholar
• Tian H, Xu R, Canadell JG, Thompson RL, Winiwarter W, Suntharalingam P, Davidson EA, Ciais P, Jackson RB, Janssens-Maenhout G, et al. 2020. A comprehensive quantification of global nitrous oxide sources and sinks. Nature. 586:248–256. doi:10.1038/s41586-020-2780-0.
   PubMed Web of Science ®Google Scholar
• Timilsina A, Zhang C, Pandey B, Bizimana F, Dong X, Hu C. 2020. Potential pathway of nitrous oxide formation in plants. Front Plant Sci. 11:1177. doi:10.3389/fpls.2020.01177.
   PubMed Web of Science ®Google Scholar
• Torres MJ, Rubia MI, de la Peña T, Pueyo JJ, Bedmar EJ, Delgado MJ. 2014. Genetic basis for denitrification in Ensifer meliloti. BMC Microbiol. 14:142–151. doi:10.1186/1471-2180-14-142.
   PubMed Web of Science ®Google Scholar
• Torres MJ, Simon J, Rowley G, Bedmar EJ, Richardson DJ, Gates AJ, Delgado MJ. 2016. Nitrous oxide metabolism in nitrate-reducing bacteria: physiology and regulatory mechanisms. Adv Microb Physiol. 68:353–432. doi:10.1016/bs.ampbs.2016.02.007.
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1007/s13199-015-0341-3.
   Web of Science ®Google Scholar
• Tortosa G, Pacheco PJ, Hidalgo-García A, Granados A, Delgado A, Mesa S, Bedmar EJ, Delgado MJ. 2020. Copper modulates nitrous oxide emissions from soybean root nodules. Environ Exp Bot. 180:104262. doi:10.1016/j.envexpbot.2020.104262.
   Web of Science ®Google Scholar
• Trung BC, Yoshida S. 1983. Improvement of Leonard jar assembly for screening of effective rhizobium. Soil Sci Plant Nutr. 29:97–100. doi:10.1080/00380768.1983.10432410.
   Web of Science ®Google Scholar
• van Spanning RJ, Richardson DJ, Ferguson SJ. 2007. Introduction to the biochemistry and molecular biology of denitrification. In: Bothe H, Ferguson SJ, Newton WE, editor. Biology of the nitrogen cycle. Amsterdam: Elsevier; p. 3–20.
   Google Scholar
• Weinstein M, Roberts RC, Helinski DR. 1992. A region of the broad-host-range plasmid RK2 causes stable in planta inheritance of plasmids in Rhizobium meliloti cells isolated from alfalfa root nodules. J Bacteriol. 174:7486–7489. doi:10.1128/jb.174.22.7486-7489.1992.
   PubMed Web of Science ®Google Scholar
• Zumft WG. 1997. Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev. 61:533–616.
   PubMed Web of Science ®Google Scholar