Nitrogen Cycling in Soybean Rhizosphere: Sources and Sinks of Nitrous Oxide (N2O)

Abstract

Nitrous oxide (N₂O) is the third most important greenhouse gas after carbon dioxide and methane, and a prominent ozone-depleting substance. Agricultural soils are the primary anthropogenic source of N₂O because of the constant increase in the use of industrial nitrogen (N) fertilizers. The soybean crop is grown on 6% of the world's arable land, and its production is expected to increase rapidly in the future. In this review, we summarize the current knowledge on N-cycle in the rhizosphere of soybean plants, particularly sources and sinks of N₂O. Soybean root nodules are the host of dinitrogen (N₂)-fixing bacteria from the genus Bradyrhizobium. Nodule decomposition is the main source of N₂O in soybean rhizosphere, where soil organisms mediate the nitrogen transformations that produce N₂O. This N₂O is either emitted into the atmosphere or further reduced to N₂ by the bradyrhizobial N₂O reductase (N₂OR), encoded by the nos gene cluster. The dominance of nos ^- indigenous populations of soybean bradyrhizobia results in the emission of N₂O into the atmosphere. Hence, inoculation with nos ⁺ or nos ⁺⁺ (mutants with enhanced N₂OR activity) bradyrhizobia has proved to be promising strategies to reduce N₂O emission in the field. We discussed these strategies, the molecular mechanisms underlying them, and the future perspectives to develop better options for global mitigation of N₂O emission from soils.

Keywords: Bradyrhizobium; N2O reductase; denitrification; greenhouse gas; mitigation strategies; nos regulation; rhizosphere; soybean.

FIGURE 1

Nitrogen transformations in soybean rhizosphere. Organic nitrogen in the nodule is mineralized into NH₄⁺ that will be transformed into N₂O through nitrification and denitrification processes. Soybean bradyrhizobia (blue) and other microorganisms contribute to the denitrification process. The N₂O formed is either emitted into the atmosphere (red) or further reduced to N₂ exclusively by soybean bradyrhizobia that produce N₂O reductase (N₂OR; blue). Nase, nitrogenase; NR, dissimilatory nitrate reductase; Nap, periplasmic nitrate reductase; NIR, dissimilatory nitrite reductase; NirK, Cu-containing nitrite reductase; NOR, nitric oxide reductase; cNor, c-type nitric oxide reductase. See text for more details.

FIGURE 2

Regulation of N₂O reductase genes in bradyrhizobia. (A) Environmental factors and regulatory proteins involved in the control of nos expression. (B) The mechanism for NasT-mediated transcriptional antitermination of the nos genes. In the absence of nitrate (NO₃^–), NasT is sequestered by NasS; thus in the absence of NasT, the native conformation of the nosR-leader mRNA, which contains the H1 and H2 hairpins, is responsible for the termination of the nos transcription. When a certain level of NO₃^– is sensed by NasS, NasT is dissociated from NasS–NasT complex; the binding of NasT to H1 (and likely to H3 region, in orange) results in a conformational change in the mRNA that allows the read-through transcription of nos genes.