An extended model for the repression of photosynthesis genes by the AppA/PpsR system in Rhodobacter sphaeroides

Abstract

Purple bacteria derive energy from aerobic respiration or photosynthesis depending on the availability of oxygen and light. Under aerobic conditions, photosynthesis genes are specifically repressed by the PpsR protein. In Rhodobacter sphaeroides, the repressive action of PpsR is antagonized by the blue‐light and redox‐sensitive flavoprotein AppA, which sequesters PpsR under anaerobic conditions into transcriptionally inactive complexes. However, under semi‐aerobic conditions, blue‐light excitation of AppA causes the AppA–PpsR complexes to dissociate, again leading to a repression of photosynthesis genes. We have recently developed a simple mathematical model suggesting that this phenotype arises from the formation of a maximum in the response curve of reduced PpsR at intermediate oxygen concentrations. However, this model focused mainly on the oxygen‐dependent interactions whereas light regulation was only implemented in a simplified manner. In the present study, we incorporate a more detailed mechanism for the light‐dependent interaction between AppA and PpsR, which now allows for a direct comparison with experiments. Specifically, we take into account that, upon blue–light excitation, AppA undergoes a conformational change, creating a long‐lived signalling state causing the dissociation of the AppA–PpsR complexes. The predictions of the extended model are found to be in good agreement with experimental results on the light‐dependent repression of photosynthesis genes under semi‐aerobic conditions. We also identify the potential kinetic and stoichiometric constraints that the interplay between light and redox regulation imposes on the functionality of the AppA/PpsR system, especially with respect to a possible bistable response.

Selective repression of light harvesting complex 2 formation in Rhodobacter azotoformans by light under semiaerobic conditions

“…And beyond that, our results of the light‐effect experiments showed that blue light was most effective in inhibiting the formation of carotenoid, BChl a , and LH2 in semiaerobically grown 134K20. Based on the observations in this study and reported by others , it was concluded that an AppA‐like protein presented in 134K20 and photosystem synthesis in semiaerobically grown 134K20 was controlled by AppA/PpsR. However, our results demonstrated that the LH2 formation was selectively repressed by blue light in semiaerobically grown 134K20.…”

Use of transcriptomic data for extending a model of the AppA/PpsR system in Rhodobacter sphaeroides

“…In order to compare the existing model [ 26 , 27 ] to experimental data (obtained from our data analysis) we had to extend the simple model [ 26 ] to include the biologically relevant input (atmospheric oxygen concentration) and output (relative levels of photosynthetic gene transcription). The output from the previous model (summarized in Additional file 1 and published elsewhere [ 26 ]) is concentration of reduced PpsR (PpsR red ) or oxidized PpsR (PpsR ox ), which is not quantifiable in vivo.…”

“…AppA is capable of sensing both oxygen and blue light using heme [ 19 , 21 ] and flavin adenine dinucleotide (FAD) cofactors, respectively [ 22 – 24 ]. It is proposed that the light and redox dependent interaction of AppA and PpsR is responsible for a phenotype in which PS gene expression is repressed by blue light under semi-aerobic conditions [ 17 , 23 , 25 – 27 ].…”

“…Recently, two mathematical models for AppA/PpsR regulation of PS gene expression in R. sphaeroides have been developed [ 26 , 27 ]. These models suggest that the phenotype where PS genes are repressed by blue light at intermediate oxygen levels will occur if PpsR is reduced on a faster time scale than AppA.…”

“…A subsequent study extended the first model [ 26 ] by incorporating a more detailed description of blue light regulation [ 27 ]. In addition to the prediction of the development of a maximum (role explained above) and bistability, the model results were compared with available data for PS gene expression inhibition at varying blue light irradiance under semi-aerobic conditions.…”