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Hydrogen production by Chlamydomonas reinhardtii: an elaborate interplay of electron sources and sinks

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Abstract

The unicellular green alga Chlamydomonas reinhardtii possesses a [FeFe]-hydrogenase HydA1 (EC 1.12.7.2), which is coupled to the photosynthetic electron transport chain. Large amounts of H2 are produced in a light-dependent reaction for several days when C. reinhardtii cells are deprived of sulfur. Under these conditions, the cells drastically change their physiology from aerobic photosynthetic growth to an anaerobic resting state. The understanding of the underlying physiological processes is not only important for getting further insights into the adaptability of photosynthesis, but will help to optimize the biotechnological application of algae as H2 producers. Two of the still most disputed questions regarding H2 generation by C. reinhardtii concern the electron source for H2 evolution and the competition of the hydrogenase with alternative electron sinks. We analyzed the H2 metabolism of S-depleted C. reinhardtii cultures utilizing a special mass spectrometer setup and investigated the influence of photosystem II (PSII)- or ribulosebisphosphate-carboxylase/oxygenase (Rubisco)-deficiency. We show that electrons for H2-production are provided both by PSII activity and by a non-photochemical plastoquinone reduction pathway, which is dependent on previous PSII activity. In a Rubisco-deficient strain, which produces H2 also in the presence of sulfur, H2 generation seems to be the only significant electron sink for PSII activity and rescues this strain at least partially from a light-sensitive phenotype. The latter indicates that the down-regulation of assimilatory pathways in S-deprived C. reinhardtii cells is one of the important prerequisites for a sustained H2 evolution.

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Abbreviations

DCMU:

3-(3,4-dichlorophenyl)-1,1-dimethylurea

FNR:

Ferredoxin-NADP+-reductase

MIMS:

Membrane inlet mass spectrometer system

PQ:

Plastoquinone

PSI:

Photosystem I

PSII:

Photosystem II

S:

Sulfur

Rubisco:

Ribulosebisphosphate-carboxylase/oxygenase

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Acknowledgments

This work was supported by DAAD (PPP with France, PROCOPE) and by the European Commission (6th FP, NEST STRP SOLAR-H contract 516510). A. Hemschemeier and T. Happe were further supported by the Deutsche Forschungsgemeinschaft (SFB 480). G. Peltier, L. Cournac and S. Fouchard were also supported by the Agence Nationale de la Recherche (projet PHOTOBIOH2).

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Correspondence to Anja Hemschemeier.

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Hemschemeier, A., Fouchard, S., Cournac, L. et al. Hydrogen production by Chlamydomonas reinhardtii: an elaborate interplay of electron sources and sinks. Planta 227, 397–407 (2008). https://doi.org/10.1007/s00425-007-0626-8

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Keywords

  • Chlamydomonas reinhardtii
  • Green algae
  • Hydrogen production
  • Photosystem II
  • Rubisco
  • Sulfur deprivation