Photosynthetic organisms need to balance the rate of photosynthesis (source activity) with the utilization of photosynthetic products by downstream reactions (sink capacity). However, cyanobacteria lack homologs to the regulatory source/sink systems well-studied in plants, making it uncertain how they sense integrated metabolic demands to coordinate upstream photosynthetic reactions to meet those energetic needs. Towards the identification of energy/sugar sensors in cyanobacteria, we utilized an engineered strain of Synechococcus elongatus PCC 7942 with a heterologous sucrose export pathway that provides an expanded and tunable metabolic sink. We conducted a comprehensive screening all two-component systems (TCS) encoded in S. elongatus by analyzing phenotypes consistent with sucrose export-induced relaxation of sink inhibition (e.g., increased photosynthetic efficiencies) in TCS knockout backgrounds. We further narrowed candidate sensor proteins by analyzing the changes observed after sucrose feeding experiments in a strain with a heterologous transporter installed, akin to classic sugar feeding experiments in plants. Taken together, we show that a clustered TCS network containing RpaA, CikB, ManS and NblS are involved in the regulation of genes related to photosynthesis, pigment synthesis, and Rubisco concentration in response to sucrose export and feeding. Analysis of the protein-protein interactome of each of these factors by proximity labeling demonstrated enrichment of enzymes involved in core metabolism and energy production. Altogether, these results highlight a regulatory TCS group that may be playing under-appreciated functions in energy balancing in photosynthetically-active cyanobacteria.