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See detailImbalance between oxygen photoreduction and antioxidant capacities in Symbiodinium cells exposed to combined heat and high light stress
Roberty, Stéphane ULg; Fransolet, David; Cardol, Pierre ULg et al

in Coral Reefs (in press)

During last decades coral reefs have been affected by several large-scale bleaching events and such phenomenon is expected to increase in frequency and severity in the future thus compromising their ... [more ▼]

During last decades coral reefs have been affected by several large-scale bleaching events and such phenomenon is expected to increase in frequency and severity in the future thus compromising their survival. High sea surface temperature accompanied by high levels of solar irradiance has been found to be responsible for the induction of an oxidative stress ultimately ending with the disruption of the symbiosis between cnidarians and Symbiodinium. Since two decades many studies have pointed out the water-water cycle as being one of the primary mediators of this phenomenon, but the impacts of environmental stress on the O2 reduction by PSI and the associated ROS-detoxifying enzymes remain to be determined. In this study, we analyzed the impacts of an acute thermal and light stress on the WWC in the model Symbiodinium strain A1. We observed that high light treatment at 26°C resulted in the up-regulation of superoxide dismutase (SOD), ascorbate peroxidase (APX) and glutathione reductase (GR) activities and an increased production of Reactive Oxygen Species (ROS) with no significant change in O2-dependent electron transport. Under high light and at 33°C, O2-dependent electron transport was significantly increased relative to total electron transport. This increase was concomitant with a two-fold increase in ROS generation compared to the treatment at 26°C, while enzymes involved in the WWC were largely inactivated. These data show for the first time that combined heat and light stress inactivate antioxidant capacities of the WWC, and suggests that its photoprotective functions are overwhelmed under these conditions. This study also indicates that cnidarians may be more prone to bleach if they harbor Symbiodinium cells having a highly active Mehler-type electron transport, unless they are able to quickly up-regulate their antioxidant capacities. [less ▲]

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See detailInduction of Photosynthetic Carbon Fixation in Anoxia Relies on Hydrogenase Activity and Proton-Gradient Regulation-Like1-Mediated Cyclic Electron Flow in Chlamydomonas reinhardtii.
Godaux, Damien ULg; Bailleul, Benjamin ULg; Berne, Nicolas ULg et al

in Plant physiology (2015), 168(2), 648-58

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 ... [more ▼]

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. [less ▲]

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See detailThe involvement of hydrogen-producing and ATP-dependent NADPH-consuming pathways in setting the redox poise in the chloroplast of Chlamydomonas reinhardtii in anoxia.
Clowez, Sophie; Godaux, Damien ULg; Cardol, Pierre ULg et al

in The Journal of biological chemistry (2015), 290(13), 8666-76

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 ... [more ▼]

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. [less ▲]

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See detailIsolation of Chlamydomonas reinhardtii mutants with altered mitochondrial respiration by chlorophyll fluorescence measurement.
Massoz, Simon; Larosa, Véronique ULg; Horrion, Bastien et al

in Journal of biotechnology (2015)

The unicellular green alga Chlamydomonas reinhardtii is a model organism for studying energetic metabolism. Most mitochondrial respiratory-deficient mutants characterized to date have been isolated on the ... [more ▼]

The unicellular green alga Chlamydomonas reinhardtii is a model organism for studying energetic metabolism. Most mitochondrial respiratory-deficient mutants characterized to date have been isolated on the basis of their reduced ability to grow in heterotrophic conditions. Mitochondrial deficiencies are usually partly compensated by adjustment of photosynthetic activity and more particularly by transition to state 2. In this work, we explored the opportunity to select mutants impaired in respiration and/or altered in dark metabolism by measuring maximum photosynthetic efficiency by chlorophyll fluorescence analyses (FV/FM). Out of about 2900 hygromycin-resistant insertional mutants generated from wild type or from a mutant strain deficient in state transitions (stt7 strain), 22 were found to grow slowly in heterotrophic conditions and 8 of them also showed a lower FV/FM value. Several disrupted coding sequences were identified, including genes coding for three different subunits of respiratory-chain complex I (NUO9, NUOA9, NUOP4) or for isocitrate lyase (ICL1). Overall, the comparison of respiratory mutants obtained in wild-type or stt7 genetic backgrounds indicated that the FV/FM value can be used to isolate mutants severely impaired in dark metabolism. [less ▲]

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See detailPSI Mehler reaction is the main alternative photosynthetic electron pathway in Symbiodinium sp., symbiotic dinoflagellates of cnidarians
Roberty, Stéphane ULg; Bailleul, Benjamin ULg; Berne, Nicolas et al

in New Phytologist (2014), 204(1), 81-91

• Photosynthetic organisms have evolved various photoprotective and regulatory mechanisms to cope with changing and high light intensities. The nature and relative amplitude of these mechanisms is matter ... [more ▼]

• Photosynthetic organisms have evolved various photoprotective and regulatory mechanisms to cope with changing and high light intensities. The nature and relative amplitude of these mechanisms is matter of debate in dinoflagellates that live in symbiosis with cnidarians. In this work, the amplitude of photosynthetic alternative electron flows to oxygen (chlororespiration, Mehler reaction, mitochondrial respiration) and PSI cyclic electron flow were investigated in Symbiodinium clades A1, B1 and F1. • Cultured Symbiodinium strains were maintained semi-continuously under identical environmental conditions. Joint measurements of oxygen evolution, fluorescence emission, and absorption changes at specific wavelengths were used to evaluate PSI and PSII electron transfer rates (ETR). • A light-dependent and O2-dependent ETR was observed in all strains. This ETR involved PSII and PSI and was insensitive to addition of mitochondrial and carbon fixation inhibitors. • These results demonstrate that photoreduction of oxygen downstream of PSI by the so-called Mehler reaction is the main alternative electron sink at the onset and steady state of photosynthesis in all strains. This mechanism in Symbiodinium sustains significant levels of photosynthetic electron flux under high light, thus acting as a photoprotective mechanism and increasing the ATP/NADPH ratio by the electron transfer chain. [less ▲]

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See detailTranscriptomics and Proteomics of a Secondary Green Alga.
Perez, Emilie ULg; Lapaille, Marie; Degand, Hervé et al

Poster (2014, August)

Euglena gracilis is a secondary green alga related to trypanosomes that derives from a secondary endosymbiosis between a phagotrophic ancestor and a prasinophycean green alga. Our general objective is to ... [more ▼]

Euglena gracilis is a secondary green alga related to trypanosomes that derives from a secondary endosymbiosis between a phagotrophic ancestor and a prasinophycean green alga. Our general objective is to study the metabolic interactions established between the secondary plastid and the mitochondrion after the endosymbiotic event and to determine the phylogenetic origin of the genes encoding the proteins involved in the energetic pathways. As a first step, we analysed the subunit composition of the mitochondrial respiratory chain, both in silico and by targeted proteomics, to assess the extent of its similitude with the respiratory chain of Trypanosomatidae. We have shown that Euglena shares many additional subunits with trypanosomes, which suggests that these subunits are not especially associated to a parasitic lifestyle. As a second step, we sequenced the total transcriptome of Euglena and determined the phylogenetic origin of each predicted transcript using a database of about 1000 complete proteomes representing the diversity of life. These analyses confirmed that Euglena recruited its genes from a very diverse set of sources. As a third step, we performed a high-throughput analysis of the mitochondrial proteome of Euglena. Our MS/MS experiments, taking advantage of the availability of our transcriptome, mostly recovered mitochondrial proteins, which indicates that our mitochondrial extracts were quite pure. The identified proteins encompassed about 15 different mitochondrial pathways. We are now in the process of comparing the expression levels of both the transcripts and the corresponding proteins across a range of culture conditions selected to differently stimulate the mitochondrion and the plastid. [less ▲]

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See detailA forward genetic screen to identify hydrogenase-deficient mutants in the unicellular green alga Chlamydomonas reinhardtii
Emonds-Alt, Barbara ULg; Godaux, Damien ULg; Cardol, Pierre ULg et al

Poster (2014, June 15)

The ability of the unicellular green alga Chlamydomonas reinhardtii to evolve molecular hydrogen (H2) is due to the presence of oxygen-sensitive Fe-hydrogenases (HydA1/2), expressed in anoxic conditions ... [more ▼]

The ability of the unicellular green alga Chlamydomonas reinhardtii to evolve molecular hydrogen (H2) is due to the presence of oxygen-sensitive Fe-hydrogenases (HydA1/2), expressed in anoxic conditions that drive the photosynthetic electron flow to reduce protons into H2. In order to identify new players involved in H2 photoproduction in Chlamydomonas, an insertion mutant library was generated using cassettes conferring resistance to hygromycin or paromomycin. Hydrogenase activity is physiologically relevant during a transition from dark anoxia to light. In dark anoxic conditions, the cellular redox poise is high and the photosynthetic electron transport chain is fully reduced. Upon illumination, hydrogenase activity allows the reoxidation of photosynthetic intersystem electron carriers until oxic conditions and carbon fixation ability are restored. We thus designed an in vivo fluorescence imaging screen based on the different kinetics of photosynthesis induction between wild type and hydrogenase-deficient mutants [1]. At this stage, three putative hydrogenase mutants have been identified on 10,000 transformants. Molecular characterization of the insertion site of the resistance cassette by TAIL-PCR and genetic analyses of the linkage between the antibiotic resistance and the fluorescence phenotype showed that one mutant was untagged with the resistance while two tagged mutants were deficient for the HydG assembly factor. [less ▲]

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See detailMitochondrial Proteomics of a Secondary Green Alga.
Perez, Emilie ULg; Degand, Hervé; Morsomme, Pierre et al

Poster (2014, May 06)

Euglena gracilis is an alga that derives from a secondary endosymbiosis with a green alga. Our general objective is to study the interactions established between the chloroplast and the mitochondrion ... [more ▼]

Euglena gracilis is an alga that derives from a secondary endosymbiosis with a green alga. Our general objective is to study the interactions established between the chloroplast and the mitochondrion during the endosymbiosic event and to determine the phylogenetic origin of the genes encoding the proteins involved in these interactions. As a first step, we performed a high-throughput analysis of the mitochondrial proteome of Euglena gracilis. Our MS/MS experiments mostly recover mitochondrial proteins representing 15 mitochondrial pathways, which indicates that our mitochondrial extracts are relatively pure, but the phylogenetic origins of the corresponding genes are surprisingly diverse. [less ▲]

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See detailStudy of an undershoot in chlorophyll fluorescence signal after a saturating pulse in PAM measurements
Fratamico, Anthony ULg; Cardol, Pierre ULg; Tocquin, Pierre ULg et al

Conference (2014, April 14)

In 1989, Larcher and Neuner have reported the observation of a sudden reversible drop in modulated chlorophyll fluorescence measurements (PAM) immediately after a saturating pulse, and called it “low ... [more ▼]

In 1989, Larcher and Neuner have reported the observation of a sudden reversible drop in modulated chlorophyll fluorescence measurements (PAM) immediately after a saturating pulse, and called it “low-wave”. 25 years later, whereas some papers reported this phenomenon as a trivial detail, scarcely two works have investigated the origin of this particular signal, in which a link with a low CO2 availability seems clear. Our work on Haematococcus pluvialis, a freshwater green microalga, provides a new point of view on this fluorescence undershoot, caused by a rapidly established non-photochemical quenching. We have demonstrated that in the light-adapted state, a low-wave after a saturating flash can be considered as a consequence of an induction process engaged in response to the brief light increase under low CO2 conditions. The non-photochemical quenching during low-waves was found to be dependent on electron transport to oxygen during the preceding flash. Moreover, in conditions in which low-waves were observed in the light-adapted state, the fluorescence induction kinetics in the first minute of lighting after dark-adaptation presented also a reversible strong drop. Nevertheless, at the stationary state, oxygen production and photochemical yield of photosystem II were not affected. Providing a better understanding of the processes underlying low-waves, our work also draws attention on the effect of CO2 concentration on the onset of photosynthesis. [less ▲]

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See detailRegulation of Electron Transport in Photosynthesis - Chapter 16
Johnson, Giles; Minagawa, Jun; Cardol, Pierre ULg et al

in Theg, Steve; Wollman, Francis-André (Eds.) Plastid Biology (2014)

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See detailLack of isocitrate lyase in Chlamydomonas leads to changes in carbon metabolism and in the response to oxidative stress under mixotrophic growth.
Plancke, Charlotte; Vigeolas, Hélène ULg; Hohner, Ricarda et al

in The Plant journal : for cell and molecular biology (2014), 77(3), 404-417

Isocitrate lyase is a key enzyme of the glyoxylate cycle. This cycle plays an essential role in cell growth on acetate, and is important for gluconeogenesis as it bypasses the two oxidative steps of the ... [more ▼]

Isocitrate lyase is a key enzyme of the glyoxylate cycle. This cycle plays an essential role in cell growth on acetate, and is important for gluconeogenesis as it bypasses the two oxidative steps of the tricarboxylic acid (TCA) cycle in which CO2 is evolved. In this paper, a null icl mutant of the green microalga Chlamydomonas reinhardtii is described. Our data show that isocitrate lyase is required for growth in darkness on acetate (heterotrophic conditions), as well as for efficient growth in the light when acetate is supplied (mixotrophic conditions). Under these latter conditions, reduced acetate assimilation and concomitant reduced respiration occur, and biomass composition analysis reveals an increase in total fatty acid content, including neutral lipids and free fatty acids. Quantitative proteomic analysis by 14 N/15 N labelling was performed, and more than 1600 proteins were identified. These analyses reveal a strong decrease in the amounts of enzymes of the glyoxylate cycle and gluconeogenesis in parallel with a shift of the TCA cycle towards amino acid synthesis, accompanied by an increase in free amino acids. The decrease of the glyoxylate cycle and gluconeogenesis, as well as the decrease in enzymes involved in beta-oxidation of fatty acids in the icl mutant are probably major factors that contribute to remodelling of lipids in the icl mutant. These modifications are probably responsible for the elevation of the response to oxidative stress, with significantly augmented levels and activities of superoxide dismutase and ascorbate peroxidase, and increased resistance to paraquat. [less ▲]

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See detailThe mitochondrial respiratory chain of the secondary green alga Euglena gracilis shares many additional subunits with parasitic Trypanosomatidae.
Perez, Emilie ULg; Lapaille, Marie; Degand, Herve et al

in Mitochondrion (2014)

The mitochondrion is an essential organelle for the production of cellular ATP in most eukaryotic cells. It is extensively studied, including in parasitic organisms such as trypanosomes, as a potential ... [more ▼]

The mitochondrion is an essential organelle for the production of cellular ATP in most eukaryotic cells. It is extensively studied, including in parasitic organisms such as trypanosomes, as a potential therapeutic target. Recently, numerous additional subunits of the respiratory-chain complexes have been described in Trypanosoma brucei and Trypanosoma cruzi. Since these subunits had apparently no counterparts in other organisms, they were interpreted as potentially associated with the parasitic trypanosome lifestyle. Here we used two complementary approaches to characterise the subunit composition of respiratory complexes in Euglena gracilis, a non-parasitic secondary green alga related to trypanosomes. First, we developed a phylogenetic pipeline aimed at mining sequence databases for identifying homologs to known respiratory-complex subunits with high confidence. Second, we used MS/MS proteomics after two-dimensional separation of the respiratory complexes by Blue Native- and SDS-PAGE to both confirm in silico predictions and to identify further additional subunits. Altogether, we identified 41 subunits that are restricted to E. gracilis, T. brucei and T. cruzi, along with 48 classical subunits described in other eukaryotes (i.e. plants, mammals and fungi). This moreover demonstrates that at least half of the subunits recently reported in T. brucei and T. cruzi are actually not specific to Trypanosomatidae, but extend at least to other Euglenozoa, and that their origin and function are thus not specifically associated with the parasitic lifestyle. Furthermore, preliminary biochemical analyses suggest that some of these additional subunits underlie the peculiarities of the respiratory chain observed in Euglenozoa. [less ▲]

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See detailInteractions of subunits Asa2, Asa4 and Asa7 in the peripheral stalk of the mitochondrial ATP synthase of the chlorophycean alga Polytomella sp.
Miranda-Astudillo, Hector; Cano-Estrada, Araceli; Vazquez-Acevedo, Miriam et al

in Biochimica et Biophysica Acta-Bioenergetics (2014), 1837

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See detailInactivation of genes coding for mitochondrial Nd7 and Nd9 complex I subunits in Chlamydomonas reinhardtii. Impact of complex I loss on respiration and energetic metabolism.
Massoz, Simon; Larosa, Véronique ULg; Plancke, Charlotte et al

in Mitochondrion (2013)

In Chlamydomonas, unlike in flowering plants, genes coding for Nd7 (NAD7/49kDa) and Nd9 (NAD9/30kDa) core subunits of mitochondrial respiratory-chain complex I are nucleus-encoded. Both genes possess all ... [more ▼]

In Chlamydomonas, unlike in flowering plants, genes coding for Nd7 (NAD7/49kDa) and Nd9 (NAD9/30kDa) core subunits of mitochondrial respiratory-chain complex I are nucleus-encoded. Both genes possess all the features that facilitate their expression and proper import of the polypeptides in mitochondria. By inactivating their expression by RNA interference or insertional mutagenesis, we show that both subunits are required for complex I assembly and activity. Inactivation of complex I impairs the cell growth rate, reduces the respiratory rate, leads to lower intracellular ROS production and lower expression of ROS scavenging enzymes, and is associated to a diminished capacity to concentrate CO2 without compromising photosynthetic capacity. [less ▲]

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See detailFunction of the Chloroplast Hydrogenase in the Microalga Chlamydomonas: The Role of Hydrogenase and State Transitions during Photosynthetic Activation in Anaerobiosis
Ghysels, Bart ULg; Godaux, Damien ULg; Matagne, René-Fernand ULg et al

in PLoS ONE (2013), 8(5), 64161

Like a majority of photosynthetic microorganisms, the green unicellular alga Chlamydomonas reinhardtii may encounter O2 deprived conditions on a regular basis. In response to anaerobiosis or in a ... [more ▼]

Like a majority of photosynthetic microorganisms, the green unicellular alga Chlamydomonas reinhardtii may encounter O2 deprived conditions on a regular basis. In response to anaerobiosis or in a respiration defective context, the photosynthetic electron transport chain of Chlamydomonas is remodeled by a state transition process to a conformation that favours the photoproduction of ATP at the expense of reductant synthesis. In some unicellular green algae including Chlamydomonas, anoxia also triggers the induction of a chloroplast-located, oxygen sensitive hydrogenase, which accepts electrons from reduced ferredoxin to convert protons into molecular hydrogen. Although microalgal hydrogen evolution has received much interest for its biotechnological potential, its physiological role remains unclear. By using specific Chlamydomonas mutants, we demonstrate that the state transition ability and the hydrogenase function are both critical for induction of photosynthesis in anoxia. These two processes are thus important for survival of the cells when they are transiently placed in an anaerobic environment. [less ▲]

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See detailA dual strategy to cope with high light in Chlamydomonas reinhardtii
Allorent, G; Tokutsu, R; Roach, T et al

in Plant Cell (2013), 25(2), 545-557

Absorption of light in excess of the capacity for photosynthetic electron transport is damaging to photosynthetic organisms. Several mechanisms exist to avoid photodamage, which are collectively referred ... [more ▼]

Absorption of light in excess of the capacity for photosynthetic electron transport is damaging to photosynthetic organisms. Several mechanisms exist to avoid photodamage, which are collectively referred to as nonphotochemical quenching. This term comprises at least two major processes. State transitions (qT) represent changes in the relative antenna sizes of photosystems II and I. High energy quenching (qE) is the increased thermal dissipation of light energy triggered by lumen acidification. To investigate the respective roles of qE and qT in photoprotection, a mutant (npq4 stt7-9) was generated in Chlamydomonas reinhardtii by crossing the state transition–deficient mutant (stt7-9) with a strain having a largely reduced qE capacity (npq4). The comparative phenotypic analysis of the wild type, single mutants, and double mutants reveals that both state transitions and qE are induced by high light. Moreover, the double mutant exhibits an increased photosensitivity with respect to the single mutants and the wild type. Therefore, we suggest that besides qE, state transitions also play a photoprotective role during high light acclimation of the cells, most likely by decreasing hydrogen peroxide production. These results are discussed in terms of the relative photoprotective benefit related to thermal dissipation of excess light and/or to the physical displacement of antennas from photosystem II. [less ▲]

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