Flavodiiron Proteins Promote Fast and Transient O₂ Photoreduction in Chlamydomonas

Abstract

During oxygenic photosynthesis, the reducing power generated by light energy conversion is mainly used to reduce carbon dioxide. In bacteria and archae, flavodiiron (Flv) proteins catalyze O 2 or NO reduction, thus protecting cells against oxidative or nitrosative stress. These proteins are found in cyanobacteria, mosses, and microalgae, but have been lost in angiosperms. Here, we used chlorophyll fluorescence and oxygen exchange measurement using [18 O]-labeled O 2 and a membrane inlet mass spectrometer to characterize Chlamydomonas reinhardtii flvB insertion mutants devoid of both FlvB and FlvA proteins. We show that Flv proteins are involved in a photo-dependent electron flow to oxygen, which drives most of the photosynthetic electron flow during the induction of photosynthesis. As a consequence, the chlorophyll fluorescence patterns are strongly affected in flvB mutants during a light transient, showing a lower PSII operating yield and a slower nonphotochemical quenching induction. Photoautotrophic growth of flvB mutants was indistinguishable from the wild type under constant light, but severely impaired under fluctuating light due to PSI photo damage. Remarkably, net photosynthesis of flv mutants was higher than in the wild type during the initial hour of a fluctuating light regime, but this advantage vanished under longterm exposure, and turned into PSI photo damage, thus explaining the marked growth retardation observed in these conditions. We conclude that the C. reinhardtii Flv participates in a Mehler-like reduction of O 2 , which drives a large part of the photosynthetic electron flow during a light transient and is thus critical for growth under fluctuating light regimes.

Flavodiiron Protein Substitutes for Cyclic Electron Flow without Competing CO2 Assimilation in Rice

“…These results indicate that FLV can be a substantial PSI electron sink (i.e. a safety valve) under fluctuating light (Chaux et al, 2017, Gerotto et al, 2016. In FLV-deficient strains of P. patens, the accumulation of PGR5 protein was up-regulated under fluctuating light, suggesting a partial compensation for the FLV function by CET-PSI (Gerotto et al, 2016).…”

Balancing protection and efficiency in the regulation of photosynthetic electron transport across plant evolution

“…). In eukaryotes, the FLVA–FLVB complex forms a heterodimer, and the oligomeric state is fundamental for protein function, since in Physcomitrella patens and C. reinhardtii the removal of one protein leads to the loss of the other (Gerotto et al ., ; Chaux et al ., ).…”

“…Mutants depleted in FLVs showed strong photosensitivity when exposed to fluctuating light, demonstrating a physiological role particularly relevant to these conditions (Gerotto et al ., ; Chaux et al ., ; Shimakawa et al ., ). As schematized in Fig.…”

“…FLVs are instead more unevenly distributed, with up to six genes found in cyanobacteria (Zhang et al ., ) involved in the photoprotection of both PSI and PSII (Allahverdiyeva et al ., ). Eukaryotic photosynthetic organisms have maintained only two genes (named FLVA and FLVB ), and molecular evidence of FLV activity has recently emerged in chlorophyte algae (Jokel et al ., ; Chaux et al ., ), nonvascular plants (Gerotto et al ., ; Shimakawa et al ., ) and gymnosperms (Ilík et al ., ), whereas the corresponding genes are not found in any known angiosperm (Fig. ).…”

“…1). In eukaryotes, the FLVA-FLVB complex forms a heterodimer, and the oligomeric state is fundamental for protein function, since in Physcomitrella patens and C. reinhardtii the removal of one protein leads to the loss of the other (Gerotto et al, 2016;Chaux et al, 2017). CEF and PCEF have been shown to play a fundamental role in PSI photoprotection; indeed, corresponding mutants showed PSI damage and sharp growth defects (Munekage et al, 2004;Takahashi et al, 2009;Suorsa et al, 2012;Gerotto et al, 2016).…”