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Nitrogen deprivation results in photosynthetic hydrogen production in Chlamydomonas reinhardtii

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Abstract

The unicellular green alga Chlamydomonas reinhardtii is able to use photosynthetically provided electrons for the production of molecular hydrogen by an [FeFe]-hydrogenase HYD1 accepting electrons from ferredoxin PetF. Despite the severe sensitivity of HYD1 towards oxygen, a sustained and relatively high photosynthetic hydrogen evolution capacity is established in C. reinhardtii cultures when deprived of sulfur. One of the major electron sources for proton reduction under this condition is the oxidation of starch and subsequent non-photochemical transfer of electrons to the plastoquinone pool. Here we report on the induction of photosynthetic hydrogen production by Chlamydomonas upon nitrogen starvation, a nutritional condition known to trigger the accumulation of large deposits of starch and lipids in the green alga. Photochemistry of photosystem II initially remained on a higher level in nitrogen-starved cells, resulting in a 2-day delay of the onset of hydrogen production compared with sulfur-deprived cells. Furthermore, though nitrogen-depleted cells accumulated large amounts of starch, both hydrogen yields and the extent of starch degradation were significantly lower than upon sulfur deficiency. Starch breakdown rates in nitrogen or sulfur-starved cultures transferred to darkness were comparable in both nutritional conditions. Methyl viologen treatment of illuminated cells significantly enhanced the efficiency of photosystem II photochemistry in sulfur-depleted cells, but had a minor effect on nitrogen-starved algae. Both the degradation of the cytochrome b 6 f complex which occurs in C. reinhardtii upon nitrogen starvation and lower ferredoxin amounts might create a bottleneck impeding the conversion of carbohydrate reserves into hydrogen evolution.

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Abbreviations

ATP:

Adenosine triphosphate

Chl:

Chlorophyll

DCMU:

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

LHCII:

Light-harvesting complex of PSII

NAD(P)H:

Nicotinamide adenine dinucleotide (phosphate)

PQ:

Plastoquinone

PSI, PSII:

Photosystem I, II

Rubisco:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

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Acknowledgments

Financial support by the BMBF (H2-Designzelle), the DAAD (Project Based Personnel Exchange Programme with Spain, contract D/06/12793), the European Union (FP7, SolarH2 Consortium) and the VW foundation (LigH2t) is gratefully acknowledged. We are furthermore very thankful for fruitful suggestions and discussions with Emilio Fernández (University of Córdoba, Spain), Laurent Cournac (CEA Cadarache, France) and Gábor Bernát (Ruhr-University of Bochum, Germany) as well as for gifts of antibodies from Francis-André Wollman (CNRS—University of Paris 6, France), Jean-David Rochaix (University of Geneva, Switzerland) and Sungsoon Park (Aurora Biofuels, USA).

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  1. AG Photobiotechnologie, Fakultät für Biologie und Biotechnologie, Lehrstuhl für Biochemie der Pflanzen, Ruhr-Universität Bochum, ND2/134, 44780, Bochum, Germany

    Anja Hemschemeier

  2. AG Photobiotechnologie, Fakultät für Biologie und Biotechnologie, Lehrstuhl für Biochemie der Pflanzen, Ruhr-Universität Bochum, ND2/132, 44780, Bochum, Germany

    Gabriele Philipps

  3. AG Photobiotechnologie, Fakultät für Biologie und Biotechnologie, Lehrstuhl für Biochemie der Pflanzen, Ruhr-Universität Bochum, ND2/169, 44780, Bochum, Germany

    Thomas Happe

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Philipps, G., Happe, T. & Hemschemeier, A. Nitrogen deprivation results in photosynthetic hydrogen production in Chlamydomonas reinhardtii . Planta 235, 729–745 (2012). https://doi.org/10.1007/s00425-011-1537-2

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