Purple phototrophic bacteria (PPB) naturally accept CO2 into their metabolism as a primary redox sink system in photo-heterotrophy. Dedicated use of this feature for developing sustainable processes (e.g., through negative-emissions photo-bioelectrosynthesis) requires a deep knowledge of the inherent metabolic mechanisms. Here we provide evidence of the tuning of the PPB metabolic mechanisms upon redox stressing through negative polarization (-0.4 and -0.8 V vs. Ag/AgCl) in photo-bioelectrochemical devices. Using metaproteomic analysis at both reactor ans species level, we showed that a mixed PPB-culture up-regulates its ability to capture CO2 from organics oxidation through the Calvin-Besson-Bassam cycle and anaplerotic pathways, and the redox imbalance is promoted to polyhydroxyalkanoates production. The ecological relationship of PPB with mutualist bacteria stabilizes the system and opens the door for future development of photo-bioelectrochemical devices focused on CO2 up-cycling.