Algal Proteins/genetics/metabolism; Chlamydomonas reinhardtii/enzymology/metabolism; Chloroplasts/enzymology; Hydrogen/metabolism; NADH Dehydrogenase/genetics/metabolism; Oxygen/metabolism; Photosynthesis/physiology; Photosystem II Protein Complex/metabolism; Starch/metabolism; Sulfur/metabolism
Abstract :
[en] The relative contributions of the PSII-dependent and Nda2-dependent pathways for H(2) photoproduction were investigated in the green microalga Chlamydomonas reinhardtii after suphur-deprivation. For this purpose, H(2) gas production was compared for wild-type and Nda2-deficient cells with or without DCMU (a PSII-inhibitor) in the same experimental conditions. Nda2-deficiency caused a 30% decrease of the maximal H(2) photoevolution rate observed shortly after the establishment of anoxia, and an acceleration of the decline of H(2) photoevolution rate with time. DCMU addition to Nda2-deficient cells completely inhibited H(2) photoproduction, showing that the PSII-independent H(2) photoproduction relies on the presence of Nda2, which feeds the photosynthetic electron transport chain with electrons derived from oxidative catabolism. Nda2-protein abundance increased as a result of sulphur deprivation and further during the H(2) photoproduction process, resulting in high rates of non-photochemical plastoquinone reduction in control cells. Nda2-deficiency had no significant effect on photosynthetic and respiratory capacities in sulphur-deprived cells, but caused changes in the cell energetic status (ATP and NADPH/NADP+ ratio). The rapid decline of H(2) photoevolution rate with time in Nda2-deficient cells revealed a more pronounced inhibition of H(2) photoproduction by accumulated H(2) in the absence of non-photochemical plastoquinone reduction. Nda2 is therefore important for linking H(2) photoproduction with catabolism of storage carbon compounds, and seems also involved in regulating the redox poise of the photosynthetic electron transport chain during H(2) photoproduction.
Angenent L.T., Karim K., Al-Dahhan M., Wrenn B.A., Domiguez-Espinoza R. Production of bioenergy and biochemicals from industrial and agricultural wastewater. Trends in Biotechnology 2004, 22:477-485.
Chochois V., Dauvillée D., Beyly A., Tolleter D., Cuiné S., Timpano H., Ball S., Cournac L., Peltier G. Hydrogen production in Chlamydomonas: photosystem II-dependent and -independent pathways differ in their requirement for starch metabolism. Plant Physiology 2009, 151:631-640.
Desplats C., Mus F., Cuiné S., Billon E., Cournac L., Peltier G. Characterization of Nda2, a plastoquinone-reducing type II NAD(P)H dehydrogenase in Chlamydomonas chloroplasts. Journal of Biological Chemistry 2009, 284:4148-4157.
Fouchard S., Hemschemeier A., Caruana A., Pruvost J., Legrand J., Happe T., Peltier G., Cournac L. Autotrophic and mixotrophic hydrogen photoproduction in sulfur-deprived Chlamydomonas cells. Applied and Environment Microbiology 2005, 71:6199-6205.
Gans P., Rebeille F. Control in the dark of the plastoquinone redox state by mitochondrial activity in Chlamydomonas reinhardtii. Biochimica et Biophysica Acta 1990, 1015:150-155.
Ghysels B., Franck F. Hydrogen photo-evolution upon S deprivation stepwise: an illustration of microalgal photosynthetic and metabolic flexibility and a step stone for future biotechnological methods of renewable H2 production. Photosynthesis Research 2010, 106:145-154.
Gorman D.S., Levine R.P. Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardtii. Proceedings of the National Academy of Sciences of the United States of America 1965, 94:3436-3441.
Houyoux P.-A., Ghysels B., Lecler R., Franck F. Interplay between non-photochemical plastoquinone reduction and re-oxidation in pre-illuminated Chlamydomonas reinhardtii: a fluorescence study. Photosynthesis Research 2011, 110:13-24.
Jans F., Mignolet E., Houyoux P.-A., Cardol P., Ghysels B., Cuiné S., Cournac L., Peltier G., Remacle C., Franck F. A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:20546-20551.
Kruse O., Rupprecht J., Bader K.P., Thomas-Hall S., Schenk P.M., Finazzi G., Hankamer B. Improved photobiological H2 production in engineered green algal cells. Journal of Biological Chemistry 2005, 280:34170-34177.
Hemschemeier A., Happe T. Alternative photosynthetic electron transport pathways during anaerobiosis in the green alga Chlamydomonas reinhardtii. Biochimica et Biophysica Acta 2011, 1804:919-926.
Hemschemeier A., Fouchard S., Cournac L., Peltier G., Happe T. Hydrogen production by Chlamydomonas reinhardtii: an elaborate interplay of electron sources and sinks. Planta 2008, 227:397-407.
Lichtenthaler H.K. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 1987, 148:350-382.
Liu D., Wong P., Dutka B. Determination of carbohydrate in lake sediment by a modified phenol-sulfuric acid method. Water Research 1973, 7:741-746.
Mandal B., Nath K., Das D. Improvement of biohydrogen production under decreased partial pressure of H2 by Enterobacter cloacae. Biotechnology Letters 2006, 28:831-835.
Masset J., Hiligsmann S., Hamilton C., Beckers L., Franck F., Thonart P. Effect of pH on glucose and starch fermentation in batch and sequenced-batch mode with a recently isolated strain of hydrogen-producing Clostridium butyricum CWBI1009. International Journal of Hydrogen Energy 2010, 35:3371-3378.
Matagne R.-F., Loppes R., Deltour R. Phosphatases of Chlamydomonas reinhardtii: biochemical and cytochemical approach with specific mutants. Journal of Bacteriology 1976, 126:937-950.
Matsumura H., Miyashi S. Cycling assay for nicotinamide adenine dinucleotides. Methods in Enzymology 1983, 69:465-470.
Melis A., Zhang L., Forestier M., Ghirardi M.L., Seibert M. Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiology 2000, 122:127-136.
Melis A., Happe T. Hydrogen production. Green algae as a source of energy. Plant Physiology 2001, 127:740-748.
Melis A. Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (unicellular green algae). Planta 2007, 226:1075-1086.
Peltier G., Tolleter D., Billon E., Cournac L. Auxiliary electron transport pathways in chloroplasts of microalgae. Photosynthesis Research 2010, 106:19-31.
Remacle C., Baurain D., Cardol P., Matagne R.F. Mutants of Chlamydomonas reinhardtii deficient in mitochondrial complex I: characterization of two mutations affecting the nd1 coding sequence. Genetics 2001, 158:1051-1060.
Srirangan K., Pyne M.E., Chou C.P. Biochemical and genetic engineering strategies to enhance hydrogen production in photosynthetic algae and cyanobacteria. Bioresource Technology 2011, 102:8589-8604.
Terashima M., Specht M., Naumann B., Hippler M. Characterizing the anaerobic response of Chlamydomonas reinhardtii by quantitative proteomics. Molecular and Cellular Proteomics 2010, 9:1514-1532.
Tolleter D., Ghysels B., Alric J., Petroutsos D., Toltstygina I., Krawietz D., Happe T., Auroy P., Adriano J.M., Beyly A., Cuiné S., Piet J., Reiter I.M., Genty B., Cournac L., Hippler M., Peltier G. Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell 2011, 23:2619-2630.
Zhang L., Happe T., Melis A. Biochemical and morphological characterization of sulfur-deprived and H2-producing Chlamydomonas reinhardtii (green alga). Planta 2002, 214:552-561.