Regulation of cyclic electron flow in Chlamydomonas reinhardtii under fluctuating carbon availability

The chloroplast must rapidly and precisely adjust photosynthetic ATP and NADPH output to meet changing metabolic demands imposed by fluctuating environmental conditions. Cyclic electron flow (CEF) around photosystem I is thought to contribute to this adjustment by providing ATP in excess of that supplied by linear electron low, balancing chloroplast energy budget when relative demand for ATP is high. We assessed the kinetics and energy production of CEF activation in Chlamydomonas reinhardtii under rapid changes of organic and inorganic carbon availability. Comparisons of transient electric field and chlorophyll fluorescence measurements indicated CEF was activated under conditions where ATP demand is expected to be high, consistent with a role in balancing the cellular ATP/NADPH budget under fluctuating environmental or metabolic conditions. CEF activation was not correlated with antenna state transitions, both in wild-type and the state transition mutant stt7-9, suggesting that CEF is rapidly regulated by allosteric or redox modulators. Comparing the CEF under ambient and high CO2 conditions suggests an increase in required energy output of approximately 1ATP/CO2 fixed, nearly sufficient to power proposed mechanistic models for the carbon-concentrating mechanism. Additionally, we see three-fold higher CEF rates in cells under steady-state conditions than cells under similar conditions with inhibited photosystem II, and up to five times higher in cells with severe depletion of inorganic carbon, implying that CEF has larger energetic capacity than predicted from some previous work.