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Microbial sulfur metabolism, particularly the formation and consumption of insoluble elemental sulfur (S(0)), is an important biogeochemical engine that has been harnessed for applications ranging from bioleaching and biomining to remediation of waste streams. Chlorobaculum tepidum , a low-light adapted photoautolithotrophic sulfur oxidizing bacterium, oxidizes multiple sulfur species and displays a preference for more reduced electron donors: sulfide > S(0) > thiosulfate. To understand this preference in the context of light energy availability, an ‘energy landscape’ of phototrophic sulfur oxidation was constructed by varying electron donor identity, light flux, and culture duration. Biomass and cellular parameters of Cba. tepidum cultures grown across this landscape were analyzed. From these data, a correction factor for colorimetric protein assays was developed, enabling more accurate biomass measurements for Cba. tepidum as well as other organisms. Cba. tepidum ’s bulk amino acid composition correlated with energy landscape parameters, including a tendency toward less energetically expensive amino acids under reduced light flux. This correlation, paired with an observation of increased cell size and storage carbon production under electron-rich growth conditions, suggests that Cba. tepidum has evolved to cope with changing energy availability by tuning its proteome for energetic efficiency and storing compounds for leaner times. IMPORTANCE: How microbes cope with and adapt to varying energy availability is an important factor in understanding microbial ecology and in designing efficient biotechnological processes. We explored the response of a model phototrophic organism, Chlorobaculum tepidum , across a factorial experimental design that enabled simultaneous variation and analysis of multiple growth conditions, what we term the ‘energy landscape’. Cba. tepidum biomass composition shifted toward less energetically expensive amino acids at low light. This observation provides experimental evidence for evolved efficiencies in microbial proteomes and emphasizes the role that energy flux may play in the adaptive responses of organisms. From a practical standpoint, our data suggest that bulk biomass amino acid composition could provide a simple proxy to monitor and identify energy stress in microbial systems.