Chloroflexus aurantiacus is a filamentous anoxygenic phototrophic bacterium that grows chemotrophically under oxic conditions and phototrophically under anoxic conditions. Because photosynthesis-related genes are scattered without any gene clusters in the genome, it is still unclear how this bacterium regulates protein expression in response to environmental changes. In this study, we performed a proteomic time-course analysis of how C. aurantiacus expresses proteins to acclimate to environmental changes, namely the transition from chemoheterotrophic respiratory to photoheterotrophic growth mode. Proteomic analysis detected a total of 2520 proteins out of 3934 coding sequences in the C. aurantiacus genome from samples collected at 13 time points. Almost all proteins for reaction centers, light-harvesting chlorosomes, and carbon fixation pathways were successfully detected during the growing phases in which optical densities and relative bacteriochlorophyll c contents increased simultaneously. Combination of proteomics and pigment analysis suggests that the self-aggregation of bacteriochlorophyllide c could precede the esterification of the hydrophobic farnesyl tail in cells. Cytoplasmic subunits of alternative complex III were interchanged between oxic and anoxic conditions, although membrane-bound subunits were used for both conditions. These data highlight the protein expression dynamics of phototrophy-related genes during the transition from respiration to phototrophy.