Aerobic Anoxygenic Phototrophic (AAP) bacteria are an important component of freshwater bacterioplankton. These organisms can support their predominantly heterotrophic metabolism with energy from light, their growth efficiency. Based on the results from cultures, it was hypothesised photoheterotrophy provides an advantage under carbon limitation and facilitates access to recalcitrant or low-energy carbon sources. However, verification of these hypotheses for natural AAP communities is lacking. Here, we conducted whole community manipulation experiments and compared the growth of AAP bacteria under carbon limited and with recalcitrant or low-energy carbon sources under dark and light conditions to elucidate how they profit from photoheterotrophy. The key finding is that it depends on the season. In spring, AAP bacteria induce photoheterotrophic metabolism under carbon limitation but over-compete heterotrophic bacteria when carbon is available. This effect seems to be driven by physiological responses rather than changes at the community level. In autumn photoheterotrophy is less beneficial. In both seasons, AAP bacteria responded negatively to recalcitrant (lignin) or low-energy (acetate) carbon sources in light. This unexpected observation may have ecosystem-level consequences as lake browning continues. In general, our findings contribute to the understanding of the dynamics of AAP bacteria observed in aquatic environments.