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The  Bradyrhizobium  sp. DOA9 strain displays the unusual properties to have a symbiotic plasmid and to fix nitrogen during both free-living and symbiotic growth. Sequence genome analysis shows that this strain contains the structural genes of dinitrogenase ( nifDK ) and the  nifA  regulatory gene on both the plasmid and chromosome. It was previously shown that both  nifDK  clusters are differentially expressed depending on growth conditions, suggesting different mechanisms of regulation. In this study, we examined the functional regulatory role of the two  nifA  genes found on the plasmid ( nifAp ) and chromosome ( nifAc ) that encode proteins with a moderate level of identity (55%) and different structural architectures. Using  gusA  (β-glucuronidase) reporter strains, we showed that both  nifA  genes were expressed during both the free-living and symbiotic growth stages. During symbiosis with  Aeschynomene americana , mutants in only one  nifA  gene were not altered in their symbiotic properties, while a double  nifA  mutant was drastically impaired in nitrogen fixation, indicating that the two NifA proteins are functionally redundant during this culture condition. In contrast, under  in vitro  conditions, the  nifAc  mutant was unable to fix nitrogen, and no effect of the  nifAp  mutation was detected, indicating that NifAc is essential to activate  nif  genes during free-living growth. In accordance, the nitrogenase fixation deficiency of this mutant could be restored by the introduction of  nifAc  but not by  nifAp  or by two chimeric  nifA  genes encoding hybrid proteins with the N-terminus part of NifAc and the C-terminus of NifAp. Furthermore, transcriptional analysis by RT-qPCR of the WT and two  nifA  mutant backgrounds showed that NifAc and NifAp activated the expression of both chromosome and plasmid structural  nifDK  genes during symbiosis, while only NifAc activated the expression of  nifDKc  during free-living conditions. In summary, this study provides a better overview of the complex mechanisms of regulation of the nitrogenase genes in the DOA9 strain that involve two distinct NifA proteins, which are exchangeable during symbiosis for the activation of  nif  genes but not during free-living growth where NifAc is essential for the activation of  nifDKc .

frontiers in microbiology

Regulation of Nitrogen Fixation in Bradyrhizobium sp. Strain DOA9 Involves Two Distinct NifA Regulatory Proteins That Are Functionally Redundant During Symbiosis but Not During Free-Living Growth