Cytochrome c6A is important for growth in fluctuating light and maintenance of the photosynthetic redox balance in Chlamydomonas reinhardtii

• Cytochrome c6 and plastocyanin are small soluble electron carriers, at least one of which is indispensable for photosynthesis. Cytochrome c6 was believed to have been lost from plants until a ubiquitous and highly conserved homologue, cytochrome c6A (c6A), was found in Arabidopsis thaliana. However, despite structural homology, c6A is unable to replace c6 in the photosynthetic electron transport chain. • The function of c6A, and why it is apparently universal in plants and green algae, remained unknown. • Here, we show that, in the green alga Chlamydomonas reinhardtii, c6A confers a growth advantage under fluctuating light and is important for maintaining the light harvesting balance between photosystems I and II in photomixotrophic conditions. • In the absence of c6A, the light harvesting balance shifts towards PSII, leading to a more reduced plastoquinone pool, abnormal cytochrome b6f redox kinetics, and increased photooxidative stress. • This study provides insights into how photosynthetic organisms acclimatize to stressful light conditions, indicating that c6A is important for this adaptation. • Based on these findings, we discuss the hypothesis of a role for c6A in thiol-based regulation in the thylakoid lumen, and propose further mechanistic studies. If correct, the proposed model would have implications for photoprotection mechanisms such as state transitions.