Complex regulatory activities associated with the histidine kinase PrrB in expression of photosynthesis genes in Rhodobacter sphaeroides 2.4.1

Rhodobacter sphaeroides 2.4.1 synthesizes a specialized photosynthetic membrane upon reduction of the O₂ tension below threshold levels. The genes prrB and prrA encode a sensor kinase and a response regulator, respectively, of a two-component regulatory system that presumably is involved in transduction of the signal(s) that monitors alterations in oxygen levels. A third gene, prrC, is also involved in this cascade of events. Previously, we described a mutant form of PrrB, namely, PrrB78 (J. M. Eraso and S. Kaplan, J. Bacteriol. 177:2695-2706, 1995), which results in aerobic expression of the photosynthetic apparatus. Here we examine three mutated forms of the prrB gene that have the potential to encode truncated polypeptides containing the N-terminal 6, 63, or 163 amino acids, respectively. The resulting mutant strains showed residual levels of the light-harvesting spectral complexes and had diminished photosynthetic growth rates at high light intensities with no discernible growth under intermediate or low light conditions. When either lacZ transcriptional fusions or direct mRNA determinations were used to monitor specific photosynthesis gene expression, all the mutant strains showed unexpectedly high levels of gene expression when compared to mutant strains affected in prrA. Conversely, when translational fusions were used to monitor photosynthesis gene expression in these mutant strains, expression of both puc and puf operons was reduced, especially puf expression. In light of these studies and those of the PrrB78 mutant, the data suggest that PrrA can be activated in situ by something other than PrrB, and it also appears that PrrB can function as a negative regulator acting through PrrA. Finally, we consider the role of the Prr regulatory system in the posttranscriptional control of photosynthesis gene expression.