Interrelated modules in cyanobacterial photosynthesis: the carbon-concentrating mechanism, photorespiration, and light perception

Inorganic carbon uptake and photorespiratory pathway genes in Fremyella are affected by the cyanobacteriochrome regulator of chromatic acclimation RcaE, suggesting that there is interplay among photorespiration, light reactions, and the CCM.Here we consider the cyanobacterial carbon-concentrating mechanism (CCM) and photorespiration in the context of the regulation of light harvesting, using a conceptual framework borrowed from engineering: modularity. Broadly speaking, biological 'modules' are semi-autonomous functional units such as protein domains, operons, metabolic pathways, and (sub)cellular compartments. They are increasingly recognized as units of both evolution and engineering. Modules may be connected by metabolites, such as NADPH, ATP, and 2PG. While the Calvin-Benson-Bassham Cycle and photorespiratory salvage pathways can be considered as metabolic modules, the carboxysome, the core of the cyanobacterial CCM, is both a structural and a metabolic module. In photosynthetic organisms, which use light cues to adapt to the external environment and which tune the photosystems to provide the ATP and reducing power for carbon fixation, light-regulated modules are critical. The primary enzyme of carbon fixation, RuBisCO, uses CO2 as a substrate, which is accumulated via the CCM. However RuBisCO also has a secondary reaction in which it utilizes O-2, a by-product of the photochemical modules, which leads to photorespiration. A complete understanding of the interplay among CCM and photorespiration is predicated on uncovering their connections to the light reactions and the regulatory factors and pathways that tune these modules to external cues. We probe this connection by investigating light inputs into the CCM and photorespiratory pathways in the chromatically acclimating cyanobacterium Fremyella diplosiphon.