A mechanistic framework for photon-to-carbon efficiency: coupling photosynthetic energy supply and light respiration in microalgae

Photon-to-biomass conversion efficiency in oxygenic phototrophs can vary widely under controlled cultivation, yet its mechanistic origin remains difficult to resolve at the system level. Here, we combine a quantified description of light attenuation and primary photochemistry with a thermodynamically constrained metabolic framework to relate reactor-scale light forcing to intracellular energetics in Chlamydomonas reinhardtii chemostats. In a near-optimal regime, the specific growth rate scales linearly with an effective photochemical input, {phi}{gamma}, defined as the rate of photochemically productive photon absorption. This identifies a physiologically relevant forcing variable at the timescale of growth and an invariant biomass yield on productive photons. Imposing this experimentally grounded constraint reveals a compatible effective energetic coupling within photosynthetic electron transport and strongly restricts the admissible photosynthesis-respiration balance. A two-dimensional growth map in the space of photochemical forcing and respiratory activity reveals a respiration-limited region and a dissipative regime in which excessive respiration lowers photon-use efficiency. Analysis of feasible sub-optimal states identifies a small set of intracellular dissipative motifs. Among them, concomitant operation of the Calvin-Benson cycle and the oxidative pentose phosphate pathway emerges as a parsimonious reaction-level mechanism for dissipative carbon recycling. Overall, the results provide an experimentally anchored framework linking productive light absorption, energetic coupling, and light respiration to photon-yield losses in a controlled phototrophic system.