The involvement of hydrogen-producing and ATP-dependent NADPH-consuming pathways in setting the redox poise in the chloroplast of Chlamydomonas reinhardtii in anoxia.
Adenosine Triphosphate/metabolism; Anaerobiosis; Chlamydomonas reinhardtii/metabolism; Chloroplasts/metabolism; Hydrogen/metabolism; NADP/metabolism; Oxidation-Reduction; Oxygen/metabolism; Photosystem I Protein Complex/metabolism; Anaerobic Glycolysis; Chlamydomonas; Electron Transfer; Hydrogenase; Oxidation-Reduction (Redox); Photosynthesis
Résumé :
[en] Photosynthetic microalgae are exposed to changing environmental conditions. In particular, microbes found in ponds or soils often face hypoxia or even anoxia, and this severely impacts their physiology. Chlamydomonas reinhardtii is one among such photosynthetic microorganisms recognized for its unusual wealth of fermentative pathways and the extensive remodeling of its metabolism upon the switch to anaerobic conditions. As regards the photosynthetic electron transfer, this remodeling encompasses a strong limitation of the electron flow downstream of photosystem I. Here, we further characterize the origin of this limitation. We show that it stems from the strong reducing pressure that builds up upon the onset of anoxia, and this pressure can be relieved either by the light-induced synthesis of ATP, which promotes the consumption of reducing equivalents, or by the progressive activation of the hydrogenase pathway, which provides an electron transfer pathway alternative to the CO2 fixation cycle.
Disciplines :
Biochimie, biophysique & biologie moléculaire
Auteur, co-auteur :
Clowez, Sophie
Godaux, Damien ; Université de Liège > Département des sciences de la vie > Génétique et physiologie des microalgues
Cardol, Pierre ; Université de Liège > Département des sciences de la vie > Génétique et physiologie des microalgues
Wollman, Francis-Andre
Rappaport, Fabrice
Langue du document :
Anglais
Titre :
The involvement of hydrogen-producing and ATP-dependent NADPH-consuming pathways in setting the redox poise in the chloroplast of Chlamydomonas reinhardtii in anoxia.
Date de publication/diffusion :
2015
Titre du périodique :
Journal of Biological Chemistry
ISSN :
0021-9258
eISSN :
1083-351X
Maison d'édition :
American Society for Biochemistry and Molecular Biology, Etats-Unis - Maryland
Volume/Tome :
290
Fascicule/Saison :
13
Pagination :
8666-76
Peer reviewed :
Peer reviewed vérifié par ORBi
Commentaire :
(c) 2015 by The American Society for Biochemistry and Molecular Biology, Inc.
Steunou, A. S., Jensen, S. I., Brecht, E., Becraft, E. D., Bateson, M. M., Kilian, O., Bhaya, D., Ward, D. M., Peters, J. W., Grossman, A. R., and Kühl, M. (2008) Regulation of nif gene expression and the energetics of N2 fixation over the diel cycle in a hot spring microbial mat. ISME J. 2, 364-378
Hemschemeier, A., and Happe, T. (2005) The exceptional photofermentative hydrogen metabolism of the green alga Chlamydomonas reinhardtii. Biochem. Soc. Trans. 33, 39-41
Mus, F., Dubini, A., Seibert, M., Posewitz, M. C., and Grossman, A. R. (2007) Anaerobic acclimation in Chlamydomonas reinhardtii: anoxic gene expression, hydrogenase induction, and metabolic pathways. J. Biol. Chem. 282, 25475-25486
Dubini, A., Mus, F., Seibert, M., Grossman, A. R., and Posewitz, M. C. (2009) Flexibility in anaerobic metabolism as revealed in a mutant of Chlamydomonas reinhardtii lacking hydrogenase activity. J. Biol. Chem. 284, 7201-7213
Yang, W., Catalanotti, C., D'Adamo, S., Wittkopp, T. M., Ingram-Smith, C. J., Mackinder, L., Miller, T. E., Heuberger, A. L., Peers, G., Smith, K. S., Jonikas, M. C., Grossman, A. R., and Posewitz, M. C. (2014) Alternative acetate production pathways in Chlamydomonas reinhardtii during dark anoxia and the dominant role of chloroplasts in fermentative acetate production. Plant Cell 26, 4499-4518
Del Campo, J. A., Quinn, J. M., and Merchant, S. (2004) Evaluation of oxygen response involving differential gene expression in Chlamydomonas reinhardtii. Methods Enzymol. 381, 604-617
Quinn, J. M., Eriksson, M., Moseley, J. L., and Merchant, S. (2002) Oxygen deficiency responsive gene expression in Chlamydomonas reinhardtii through a copper-sensing signal transduction pathway. Plant Physiol. 128, 463-471
Hemschemeier, A., and Happe, T. (2011) Alternative photosynthetic electron transport pathways during anaerobiosis in the green alga Chlamydomonas reinhardtii. Biochim Biophys Acta 1807, 919-926
Grossman, A. R., Croft, M., Gladyshev, V. N., Merchant, S. S., Posewitz, M. C., Prochnik, S., and Spalding, M. H. (2007) Novel metabolism in Chlamydomonas through the lens of genomics. Curr. Opin. Plant Biol. 10, 190-198
Terashima, M., Specht, M., Naumann, B., and Hippler, M. (2010) Characterizing the anaerobic response of Chlamydomonas reinhardtii by quantitative proteomics. Mol. Cell. Proteomics 9, 1514-1532
Hemschemeier, A., Melis, A., and Happe, T. (2009) Analytical approaches to photobiological hydrogen production in unicellular green algae. Photosynth. Res. 102, 523-540
Wollman, F.-A., and Bulté, L. (1989) Towards an Understanding of the Physiological Role of State Transitions (Hall, D. O., and Grassi, G., eds) pp. 198-207, Elsevier, Amsterdam
Bulté, L., Gans, P., Rebeille, F., and Wollman, F.-A. (1990) ATP control on state transitions in vivo in Chlamydomonas reinhardtii. Biochim. Biophys. Acta 1020, 72-80
Jans, F., Mignolet, E., Houyoux, P. A., Cardol, P., Ghysels, B., Cuiné, S., Cournac, L., Peltier, G., Remacle, C., and Franck, F. (2008) A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. Proc. Natl. Acad. Sci. U.S.A. 105, 20546-20551
Houille-Vernes, L., Rappaport, F., Wollman, F. A., Alric, J., and Johnson, X. (2011) Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas. Proc. Natl. Acad. Sci. U.S.A. 108, 20820-20825
Bonaventura, C., and Myers, J. (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim. Biophys. Acta 189, 366-383
Vallon, O., Bulte, L., Dainese, P., Olive, J., Bassi, R., and Wollman, F.-A. (1991) Lateral redistribution of cytochrome b6/f complexes along thylakoid membranes upon state transitions. Proc. Natl. Acad. Sci. U.S.A. 88, 8262-8266
Wollman, F. A., and Lemaire, C. (1988) Studies on kinase-controlled state transitions in Photosystem II and b6f mutants from Chlamydomonas reinhardtii which lack quinone-binding proteins. Biochim. Biophys. Acta 933, 85-94
Delosme, R., Olive, J., and Wollman, F. A. (1996) Changes in light energydistribution upon state transitions-an in vivo photoacoustic study of the wild-type and photosynthesis mutants from Chlamydomonas reinhardtii. Biochim. Biophys. Acta 1273, 150-158
Iwai, M., Yokono, M., Inada, N., and Minagawa, J. (2010) Live-cell imaging of photosystem II antenna dissociation during state transitions. Proc. Natl. Acad. Sci. U.S.A. 107, 2337-2342
Nagy, G., Ünnep, R., Zsiros, O., Tokutsu, R., Takizawa, K., Porcar, L., Moyet, L., Petroutsos, D., Garab, G., Finazzi, G., and Minagawa, J. (2014) Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by noninvasive techniques in vivo. Proc. Natl. Acad. Sci. U.S.A. 111, 5042-5047
Ünlü, C., Drop, B., Croce, R., and van Amerongen, H. (2014) State transitions in Chlamydomonas reinhardtii strongly modulate the functional size of photosystem II but not of photosystem I. Proc. Natl. Acad. Sci. U.S.A. 111, 3460-3465
Finazzi, G., Furia, A., Barbagallo, R. P., and Forti, G. (1999) State transitions, cyclic and linear electron transport and photophosphorylation in Chlamydomonas reinhardtii. Biochim. Biophys. Acta 1413, 117-129
Finazzi, G., Rappaport, F., Furia, A., Fleischmann, M., Rochaix, J. D., Zito, F., and Forti, G. (2002) Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii. EMBO Rep. 3, 280-285
Terashima, M., Petroutsos, D., Hüdig, M., Tolstygina, I., Trompelt, K., Gäbelein, P., Fufezan, C., Kudla, J., Weinl, S., Finazzi, G., and Hippler, M. (2012) Calcium-dependent regulation of cyclic photosynthetic electron transfer by a CAS, ANR1, and PGRL1 complex. Proc. Natl. Acad. Sci. U.S.A. 109, 17717-17722
Takahashi, H., Clowez, S., Wollman, F. A., Vallon, O., and Rappaport, F. (2013) Cyclic electron flow is redox-controlled but independent of state transition. Nat. Commun. 4, 1954
Wollman, F. A. (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J. 20, 3623-3630
Lucker, B., and Kramer, D. M. (2013) Regulation of cyclic electron flow in Chlamydomonas reinhardtii under fluctuating carbon availability. Photosynth. Res. 117, 449-459
Alric, J. (2014) Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii: (II) involvement of the PGR5-PGRL1 pathway under anaerobic conditions. Biochim. Biophys. Acta 1837, 825-834
Iwai, M., Takizawa, K., Tokutsu, R., Okamuro, A., Takahashi, Y., and Minagawa, J. (2010) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464, 1210-1213
Ghysels, B., Godaux, D., Matagne, R. F., Cardol, P., and Franck, F. (2013) Function of the chloroplast hydrogenase in the microalga Chlamydomonas: the role of hydrogenase and state transitions during photosynthetic activation in anaerobiosis. PloS one 8, e64161
Klughammer, C., and Schreiber, U. (1994) An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. Planta 192, 261-268
Catalanotti, C., Dubini, A., Subramanian, V., Yang, W., Magneschi, L., Mus, F., Seibert, M., Posewitz, M. C., and Grossman, A. R. (2012) Altered fermentative metabolism in Chlamydomonas reinhardtii mutants lacking pyruvate formate lyase and both pyruvate formate lyase and alcohol dehydrogenase. Plant Cell 24, 692-707
Lemaire, C., and Wollman, F. A. (1989) The chloroplast ATP synthase in Chlamydomonas reinhardtii. II. Biochemical studies on its biogenesis using mutants defective in photophosphorylation. J. Biol. Chem. 264, 10235-10242
Johnson, X., Wostrikoff, K., Finazzi, G., Kuras, R., Schwarz, C., Bujaldon, S., Nickelsen, J., Stern, D. B., Wollman, F. A., and Vallon, O. (2010) MRL1, a conserved pentatricopeptide repeat protein, is required for stabilization of rbcL mRNA in Chlamydomonas and Arabidopsis. Plant Cell 22, 234-248
Quinn, J., Li, H. H., Singer, J., Morimoto, B., Mets, L., Kindle, K., and Merchant, S. (1993) The plastocyanin-deficient phenotype of Chlamydomonas reinhardtii Ac-208 results from a frame-shift mutation in the nuclear gene encoding preapoplastocyanin. J. Biol. Chem. 268, 7832-7841
Zito, F., Finazzi, G., Delosme, R., Nitschke, W., Picot, D., and Wollman, F. A. (1999) The Qo site of cytochrome b6f complexes controls the activation of the LHCII kinase. EMBO J. 18, 2961-2969
Rimbault, B., Esposito, D., Drapier, D., Choquet, Y., Stern, D., and Wollman, F. A. (2000) Identification of the initiation codon for the atpB gene in Chlamydomonas chloroplasts excludes translation of a precursor form of the β subunit of the ATP synthase. Mol. Gen. Genet. 264, 486-491
Cardol, P., Gloire, G., Havaux, M., Remacle, C., Matagne, R., and Franck, F. (2003) Photosynthesis and state transitions in mitochondrial mutants of Chlamydomonas reinhardtii affected in respiration. Plant Physiol. 133, 2010-2020
Posewitz, M. C., King, P. W., Smolinski, S. L., Zhang, L., Seibert, M., and Ghirardi, M. L. (2004) Discovery of two novel radical S-adenosylmethionine proteins required for the assembly of an active [Fe] hydrogenase. J. Biol. Chem. 279, 25711-25720
Godaux, D., Emoncls-Alt, B., Berne, N., Ghysels, B., Alric, J., Remacle, C., and Cardol, P. (2013)Anovel screening method for hydrogenase-deficient mutants in Chlamydomonas reinhardtii based on in vivo chlorophyll fluorescence and photosystem II quantum yield. Int. J. Hydrog. Energy 38, 1826-1836
Harris, E. H. (1989) The Chlamydomonas Sourcebook, pp. 25-64, Academic Press, San Diego
Junge, W., and Witt, H. T. (1968) On the ion transport system of photosynthesis-investigations on a molecular level. Z. Naturforsch. B. 23, 244-254
Finazzi, G., and Rappaport, F. (1998) In vivo characterization of the electrochemical proton gradient generated in darkness in green algae and its kinetic effects on cytochrome b6f turnover. Biochemistry 37, 9999-10005
Sacksteder, C. A., and Kramer, D. M. (2000) Dark-interval relaxation kinetics (DIRK) of absorbance changes as a quantitative probe of steadystate electron transfer. Photosynth. Res. 66, 145-158
de Lacroix de Lavalette, A., Barucq, L., Alric, J., Rappaport, F., and Zito, F. (2009) Is the redox state of the ci heme of the cytochrome b6f complex dependent on the occupation and structure of the Qi site and vice versa? J. Biol. Chem. 284, 20822-20829
Baker, N. R., Harbinson, J., and Kramer, D. M. (2007) Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant Cell Environ. 30, 1107-1125
Hiyama, T., and Ke, B. (1971) A further study of P430: a possible primary electron acceptor of photosystem I. Arch. Biochem. Biophys. 147, 99-108
Brettel, K. (1997) Electron transfer and arrangement of the redox cofactors in photosystem I. Biochim. Biophys. Acta 1318, 322-373
Joliot, P., and Joliot, A. (1985) Slow electrogenic phase and intersystem electron transfer in algae. Biochim. Biophys. Acta 806, 398-409
Kramer, D. M., and Crofts, A. R. (1993) The concerted reduction of the high-potential and low-potential chains of the bf complex by plastoquinol. Biochim. Biophys. Acta 1183, 72-84
Finazzi, G., Büschlen, S., de Vitry, C., Rappaport, F., Joliot, P., and Wollman, F. A. (1997) Function-directed mutagenesis of the cytochrome b6f complex in Chlamydomonas reinhardtii: involvement of the cd loop of cytochrome b6 in quinol binding to the Q(o) site. Biochemistry 36, 2867-2874
Schöttler, M. A., Kirchhoff, H., and Weis, E. (2004) The role of plastocyanin in the adjustment of the photosynthetic electron transport to the carbon metabolism in tobacco. Plant Physiol. 136, 4265-4274
Cammack, R., Rao, K. K., Bargeron, C. P., Hutson, K. G., Andrew, P. W., and Rogers, L. J. (1977) Midpoint redox potentials of plant and algal ferredoxins. Biochem. J. 168, 205-209
Cassan, N., Lagoutte, B., and Sétif, P. (2005) Ferredoxin-NADP+ reductase. Kinetics of electron transfer, transient intermediates, and catalytic activities studied by flash-absorption spectroscopy with isolated photosystem I and ferredoxin. J. Biol. Chem. 280, 25960-25972
Böhme, H. (1978) Quantitative determination of ferredoxin, ferredoxin- NADP+ reductase and plastocyanin in spinach chloroplasts. Eur. J. Biochem. 83, 137-141
Moal, G., and Lagoutte, B. (2012) Photo-induced electron transfer from photosystem I to NADP(+): characterization and tentative simulation of the in vivo environment. Biochim. Biophys. Acta 1817, 1635-1645
Antal, T. K., Kovalenko, I. B., Rubin, A. B., and Tyystjärvi, E. (2013) Photosynthesis- related quantities for education and modeling. Photosynth. Res. 117, 1-30
Maughan, S. C., Pasternak, M., Cairns, N., Kiddle, G., Brach, T., Jarvis, R., Haas, F., Nieuwland, J., Lim, B., Müller, C., Salcedo-Sora, E., Kruse, C., Orsel, M., Hell, R., Miller, A. J., et al. (2010) Plant homologs of the Plasmodium falciparum chloroquine-resistance transporter, PfCRT, are required for glutathione homeostasis and stress responses. Proc. Natl. Acad. Sci. U.S.A. 107, 2331-2336
Woessner, J. P., Masson, A., Harris, E. H., Bennoun, P., Gillham, N. W., and Boynton, J. E. (1984) Molecular and genetic-analysis of the chloroplast ATPase of chlamydomonas. Plant Mol. Biol. 3, 177-190
Bassham, J. A., Benson, A. A., and Calvin, M. (1950) The path of carbon in photosynthesis. J. Biol. Chem. 185, 781-787
Miller, A. G., and Canvin, D. T. (1989) Glycolaldehyde inhibits CO(2) fixation in the Cyanobacterium Synechococcus UTEX 625 without inhibiting the accumulation of inorganic carbon or the associated quenching of chlorophyll a fluorescence. Plant Physiol. 91, 1044-1049
Takahashi, S., and Murata, N. (2005) Interruption of the Calvin cycle inhibits the repair of photosystem II from photodamage. Biochim. Biophys. Acta 1708, 352-361
Joliot, P., Béal, D., and Joliot, A. (2004) Cyclic electron flow under saturating excitation of dark-adapted Arabidopsis leaves. Biochim. Biophys. Acta 1656, 166-176
Bendall, D. S., and Manasse, R. S. (1995) Cyclic photophosphorylation and electron transport. Biochim. Biophys. Acta 1229, 23-38
Allen, J. F. (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci. 8, 15-19
Alric, J., Lavergne, J., and Rappaport, F. (2010) Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii (I) aerobic conditions. Biochim. Biophys. Acta 1797, 44-51
Johnson, X., and Alric, J. (2012) Interaction between starch breakdown, acetate assimilation, and photosynthetic cyclic electron flow in Chlamydomonas reinhardtii. J. Biol. Chem. 287, 26445-26452
Melis, A., Zhang, L., Forestier, M., Ghirardi, M. L., and Seibert, M. (2000) Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol. 122, 127-136
Kuchenreuther, J. M., Britt, R. D., and Swartz, J. R. (2012) New insights into [FeFe] hydrogenase activation and maturase function. PLoS One 7, e45850
Forestier, M., King, P., Zhang, L., Posewitz, M., Schwarzer, S., Happe, T., Ghirardi, M. L., and Seibert, M. (2003) Expression of two [Fe]-hydrogenases in Chlamydomonas reinhardtii under anaerobic conditions. Eur. J. Biochem. 270, 2750-2758
Subramanian, V., Dubini, A., Astling, D. P., Laurens, L. M., Old, W. M., Grossman, A. R., Posewitz, M. C., and Seibert, M. (2014) Profiling chlamydomonas metabolism under dark, anoxic H-producing conditions using a combined proteomic, transcriptomic, and metabolomic approach. J. Proteome Res. 13, 5431-5451
Leister, D., and Shikanai, T. (2013) Complexities and protein complexes in the antimycin A-sensitive pathway of cyclic electron flow in plants. Front. Plant Sci. 4, 161
Joliot, P., and Joliot, A. (2005) Quantification of cyclic and linear flows in plants. Proc. Natl. Acad. Sci. U.S.A. 102, 4913-4918
Roach, T., and Krieger-Liszkay, A. (2014) Regulation of photosynthetic electron transport and photoinhibition. Curr. Protein Pept. Sci. 15, 351-362
Miyake, C. (2010) Alternative electron flows (water-water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. Plant Cell Physiol. 51, 1951-1963
Armbruster, U., Carrillo, L. R., Venema, K., Pavlovic, L., Schmidtmann, E., Kornfeld, A., Jahns, P., Berry, J. A., Kramer, D. M., and Jonikas, M. C. (2014) Ion antiport accelerates photosynthetic acclimation in fluctuating light environments. Nat. Commun. 5, 5439
Carraretto, L., Formentin, E., Teardo, E., Checchetto, V., Tomizioli, M., Morosinotto, T., Giacometti, G. M., Finazzi, G., and Szabó, I. (2013) A thylakoid-located two-pore K+ channel controls photosynthetic light utilization in plants. Science 342, 114-118
Tikkanen, M., and Aro, E. M. (2014) Integrative regulatory network of plant thylakoid energy transduction. Trends Plant Sci. 19, 10-17
Kramer, D. M., and Evans, J. R. (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol. 155, 70-78
Alric, J. (2010) Cyclic electron flow around photosystem I in unicellular green algae. Photosynth. Res. 106, 47-56
