Flavodiiron-Mediated O2 Photoreduction Links H2 Production with CO2 Fixation during the Anaerobic Induction of Photosynthesis

Burlacot, Adrien; Sawyer, Anne; Cuiné, Stéphan; Auroy, Pascaline; Blangy, Stéphanie; Happe, Thomas; Peltier, Gilles

doi:10.1104/pp.18.00721

Cited by 48 publications

(46 citation statements)

References 43 publications

(11 reference statements)

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“…Similar roles of CEF and FLV have been recently reported in the case of the green freshwater alga Chlamydomonas reinhardtii (Jokel et al, ). In this organism, however, CEF activity is mainly active in low‐oxygen/anaerobic conditions (Finazzi, Furia, Barbagallo, & Forti, ; Takahashi, Clowez, Wollman, Vallon, & Rappaport, ), where FLV are still active but cannot evacuate alone all the electrons in excess generated by photosynthesis (Burlacot et al, ).…”

Section: Discussionmentioning

confidence: 99%

Role of cyclic and pseudo‐cyclic electron transport in response to dynamic light changes in Physcomitrella patens

Storti

Alboresi

Gerotto

et al. 2018

Plant Cell & Environment

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Photosynthetic organisms support cell metabolism by harvesting sunlight and driving the electron transport chain at the level of thylakoid membranes. Excitation energy and electron flow in the photosynthetic apparatus is continuously modulated in response to dynamic environmental conditions. Alternative electron flow around photosystem I plays a seminal role in this regulation contributing to photoprotection by mitigating overreduction of the electron carriers. Different pathways of alternative electron flow coexist in the moss Physcomitrella patens, including cyclic electron flow mediated by the PGRL1/PGR5 complex and pseudo-cyclic electron flow mediated by the flavodiiron proteins FLV. In this work, we generated P. patens plants carrying both pgrl1 and flva knock-out mutations. A comparative analysis of the WT, pgrl1, flva, and pgrl1 flva lines suggests that cyclic and pseudo-cyclic processes have a synergic role in the regulation of photosynthetic electron transport. However, although both contribute to photosystem I protection from overreduction by modulating electron flow following changes in environmental conditions, FLV activity is particularly relevant in the first seconds after a light change whereas PGRL1 has a major role upon sustained strong illumination.

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Section: Discussionmentioning

confidence: 99%

Role of cyclic and pseudo‐cyclic electron transport in response to dynamic light changes in Physcomitrella patens

Storti

Alboresi

Gerotto

et al. 2018

Plant Cell & Environment

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“…Afterwards, P700 is oxidized, as shown in Figures 5 and 6. From cyanobacteria to gymnosperms, in the evolution of green lineage oxygenic photosynthetic organisms, flavodiiron protein (FLV) drives O 2 -dependent electron flow in the photosynthetic electron transport system, in addition to the photorespiration pathway [88][89][90][94][95][96]. FLV reduces O 2 to H 2 O using NADPH as the electron donor [88].…”

Section: Relationship Between Photorespiration-and Flavodiiron Proteimentioning

confidence: 99%

Molecular Mechanism of Oxidation of P700 and Suppression of ROS Production in Photosystem I in Response to Electron-Sink Limitations in C3 Plants

Miyake

2020

Antioxidants

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Photosynthesis fixes CO2 and converts it to sugar, using chemical-energy compounds of both NADPH and ATP, which are produced in the photosynthetic electron transport system. The photosynthetic electron transport system absorbs photon energy to drive electron flow from Photosystem II (PSII) to Photosystem I (PSI). That is, both PSII and PSI are full of electrons. O2 is easily reduced to a superoxide radical (O2−) at the reducing side, i.e., the acceptor side, of PSI, which is the main production site of reactive oxygen species (ROS) in photosynthetic organisms. ROS-dependent inactivation of PSI in vivo has been reported, where the electrons are accumulated at the acceptor side of PSI by artificial treatments: exposure to low temperature and repetitive short-pulse (rSP) illumination treatment, and the accumulated electrons flow to O2, producing ROS. Recently, my group found that the redox state of the reaction center of chlorophyll P700 in PSI regulates the production of ROS: P700 oxidation suppresses the production of O2− and prevents PSI inactivation. This is why P700 in PSI is oxidized upon the exposure of photosynthesis organisms to higher light intensity and/or low CO2 conditions, where photosynthesis efficiency decreases. In this study, I introduce a new molecular mechanism for the oxidation of P700 in PSI and suppression of ROS production from the robust relationship between the light and dark reactions of photosynthesis. The accumulated protons in the lumenal space of the thylakoid membrane and the accumulated electrons in the plastoquinone (PQ) pool drive the rate-determining step of the P700 photo-oxidation reduction cycle in PSI from the photo-excited P700 oxidation to the reduction of the oxidized P700, thereby enhancing P700 oxidation.

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“…In order to determine the contribution of FLVs to NO photoreduction, we analyzed NO and N 2 O exchange during dark to light transients in three previously characterized flvB mutants (22). These mutants are impaired in the accumulation of both FLVB and FLVA subunits (22,25,26). In the dark, no significant difference in neither NO reduction nor in N 2 O production were found between the three flvB mutants as compared to the control ( Fig.…”

Section: Light-dependent N 2 O Photoproduction Mostly Relies On Flvsmentioning

confidence: 99%

Algal photosynthesis converts nitric oxide into nitrous oxide

Burlacot

Richaud

Gosset

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Nitrous oxide (N2O), a potent greenhouse gas in the atmosphere, is produced mostly from aquatic ecosystems, to which algae substantially contribute. However, mechanisms of N2O production by photosynthetic organisms are poorly described. Here we show that the green microalga Chlamydomonas reinhardtii reduces NO into N2O using the photosynthetic electron transport. Through the study of C. reinhardtii mutants deficient in flavodiiron proteins (FLVs) or in a cytochrome p450 (CYP55), we show that FLVs contribute to NO reduction in the light, while CYP55 operates in the dark. Both pathways are active when NO is produced in vivo during the reduction of nitrites and participate in NO homeostasis. Furthermore, NO reduction by both pathways is restricted to chlorophytes, organisms particularly abundant in ocean N2O-producing hot spots. Our results provide a mechanistic understanding of N2O production in eukaryotic phototrophs and represent an important step toward a comprehensive assessment of greenhouse gas emission by aquatic ecosystems.

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Flavodiiron-Mediated O₂ Photoreduction Links H₂ Production with CO₂ Fixation during the Anaerobic Induction of Photosynthesis

Cited by 48 publications

References 43 publications

Role of cyclic and pseudo‐cyclic electron transport in response to dynamic light changes in Physcomitrella patens

Role of cyclic and pseudo‐cyclic electron transport in response to dynamic light changes in Physcomitrella patens

Molecular Mechanism of Oxidation of P700 and Suppression of ROS Production in Photosystem I in Response to Electron-Sink Limitations in C3 Plants

Algal photosynthesis converts nitric oxide into nitrous oxide

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