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Denitrification in the soybean endosymbiont  Bradyrhizobium diazoefficiens  is controlled by a complex regulatory network composed of two hierarchical cascades, FixLJ-FixK 2 -NnrR and RegSR-NifA. In the former cascade, the CRP/FNR-type transcription factors FixK 2  and NnrR exert disparate control on expression of core denitrifying systems encoded by  napEDABC ,  nirK ,  norCBQD , and  nosRZDFYLX  genes in response to microoxia and nitrogen oxides, respectively. To identify additional genes controlled by NnrR and involved in the denitrification process in  B. diazoefficiens , we compared the transcriptional profile of an  nnrR  mutant with that of the wild type, both grown under anoxic denitrifying conditions. This approach revealed more than 170 genes were simultaneously induced in the wild type and under the positive control of NnrR. Among them, we found the  cycA  gene which codes for the  c  550  soluble cytochrome (CycA), previously identified as an intermediate electron donor between the  bc  1  complex and the denitrifying nitrite reductase NirK. Here, we demonstrated that CycA is also required for nitrous oxide reductase activity. However, mutation in  cycA  neither affected  nosZ  gene expression nor NosZ protein steady-state levels. Furthermore,  cycA ,  nnrR  and its proximal divergently oriented  nnrS  gene, are direct targets for FixK 2  as determined by  in vitro  transcription activation assays. The dependence of  cycA  expression on FixK 2  and NnrR in anoxic denitrifying conditions was validated at transcriptional level, determined by quantitative reverse transcription PCR, and at the level of protein by performing heme  c -staining of soluble cytochromes. Thus, this study expands the regulon of NnrR and demonstrates the role of CycA in the activity of the nitrous oxide reductase, the key enzyme for nitrous oxide mitigation.

Expanding the Regulon of the Bradyrhizobium diazoefficiens NnrR Transcription Factor: New Insights Into the Denitrification Pathway