The model green microalga Chlamydomonas reinhardtii is frequently subject to periods of dark and
anoxia in its natural environment. Here, by resorting to mutants defective in the maturation of the chloroplastic
oxygen-sensitive hydrogenases or in
Proton-Gradient Regulation-Like1 (PGRL1)-dependent cyclic electron flow around
photosystem I (PSI-CEF), we demonstrate the sequential contribution of these alternative electron flows (AEFs) in the reactivation of photosynthetic carbon fixation during a shift from dark
anoxia to light. At light onset,
hydrogenase activity sustains a linear electron flow from
photosystem II, which is followed by a transient PSI-CEF in the wild type. By promoting
ATP synthesis without net generation of photosynthetic
reductants, the two
AEF are critical for restoration of the capacity for
carbon dioxide fixation in the light. Our data also suggest that the decrease in
hydrogen evolution with time of illumination might be due to competition for reduced
ferredoxins between
ferredoxin-
NADP(+)
oxidoreductase and hydrogenases, rather than due to the sensitivity of
hydrogenase activity to
oxygen. Finally, the absence of the two alternative pathways in a double mutant pgrl1
hydrogenase maturation factor G-2 is detrimental for photosynthesis and growth and cannot be compensated by any other
AEF or anoxic metabolic responses. This highlights the role of
hydrogenase activity and PSI-CEF in the ecological success of microalgae in low-
oxygen environments.