Alternative outlets for sustaining photosynthetic electron transport during dark-to-light transitions

Abstract

Significance Most forms of life on Earth cannot exist without photosynthesis. Our food and atmosphere depend on it. To obtain high photosynthetic yields, light energy must be efficiently coupled to the fixation of CO2 into organic molecules. Suboptimal environmental conditions can severely impact the conversion of light energy to biomass and lead to reactive oxygen production, which in turn can cause cellular damage and loss of productivity. Hence, plants, algae, and photosynthetic bacteria have evolved a network of alternative outlets to sustain the flow of photosynthetically derived electrons. Our work is focused on the nature and integration of these outlets, which will inform a rational engineering of crop plants and algae to optimize photosynthesis and meet the increased global demand for food. Environmental stresses dramatically impact the balance between the production of photosynthetically derived energetic electrons and Calvin–Benson–Bassham cycle (CBBC) activity; an imbalance promotes accumulation of reactive oxygen species and causes cell damage. Hence, photosynthetic organisms have developed several strategies to route electrons toward alternative outlets that allow for storage or harmless dissipation of their energy. In this work, we explore the activities of three essential outlets associated with Chlamydomonas reinhardtii photosynthetic electron transport: (i) reduction of O2 to H2O through flavodiiron proteins (FLVs) and (ii) plastid terminal oxidases (PTOX) and (iii) the synthesis of starch. Real-time measurements of O2 exchange have demonstrated that FLVs immediately engage during dark-to-light transitions, allowing electron transport when the CBBC is not fully activated. Under these conditions, we quantified maximal FLV activity and its overall capacity to direct photosynthetic electrons toward O2 reduction. However, when starch synthesis is compromised, a greater proportion of the electrons is directed toward O2 reduction through both the FLVs and PTOX, suggesting an important role for starch synthesis in priming/regulating CBBC and electron transport. Moreover, partitioning energized electrons between sustainable (starch; energetic electrons are recaptured) and nonsustainable (H2O; energetic electrons are not recaptured) outlets is part of the energy management strategy of photosynthetic organisms that allows them to cope with the fluctuating conditions encountered in nature. Finally, unmasking the repertoire and control of such energetic reactions offers new directions for rational redesign and optimization of photosynthesis to satisfy global demands for food and other resources.