Induction of Photosynthetic Carbon Fixation in Anoxia Relies on Hydrogenase Activity and Proton-Gradient Regulation-Like1-Mediated Cyclic Electron Flow in Chlamydomonas reinhardtii.
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.
Department of Life Sciences, Genetics and Physiology of Microalgae, PhytoSYSTEMS, University of Liège, B-4000 Liège, Belgium.
Damien
http://orcid.org/0000-0002-8699-0927
D
Godaux
Department of Life Sciences, Genetics and Physiology of Microalgae, PhytoSYSTEMS, University of Liège, B-4000 Liège, Belgium.
Benjamin
B
Bailleul
Department of Life Sciences, Genetics and Physiology of Microalgae, PhytoSYSTEMS, University of Liège, B-4000 Liège, Belgium.
Nicolas
N
Berne
Department of Life Sciences, Genetics and Physiology of Microalgae, PhytoSYSTEMS, University of Liège, B-4000 Liège, Belgium pierre.cardol@ulg.ac.be.
Pierre
http://orcid.org/0000-0001-9799-0546
P
Cardol
D000693:Anaerobiosis / Q000528:radiation effects; D057486:Carbon Cycle / Q000528:radiation effects; D002470:Cell Survival / Q000528:radiation effects; D016825:Chlamydomonas reinhardtii / Q000166:cytology / Q000254:growth & development / Q000502:physiology* / Q000528:radiation effects; D004579:Electron Transport / Q000528:radiation effects; D005287:Ferredoxin-NADP Reductase / Q000378:metabolism; D006859:Hydrogen / Q000378:metabolism; D006864:Hydrogenase / Q000378:metabolism*; D008027:Light; D008954:Models, Biological; D010788:Photosynthesis / Q000528:radiation effects; D045331:Photosystem I Protein Complex / Q000378:metabolism; D045332:Photosystem II Protein Complex / Q000378:metabolism; D010940:Plant Proteins / Q000378:metabolism*; D011522:Protons; D013213:Starch / Q000378:metabolism
D045331:Photosystem I Protein Complex; D045332:Photosystem II Protein Complex; D010940:Plant Proteins; D011522:Protons; D006859:Hydrogen; D013213:Starch; D006864:Hydrogenase; D005287:Ferredoxin-NADP Reductase