A light switch based on protein S-nitrosylation fine-tunes photosynthetic light-harvesting in the microalga Chlamydomonas reinhardtii

Abstract

Photosynthetic eukaryotes are challenged by a fluctuating light supply, demanding for a modulated expression of nucleus-encoded light-harvesting proteins associated with photosystem II (LHCII) to adjust light-harvesting capacity to the prevailing light conditions. Here, we provide clear evidence for a regulatory circuit that controls cytosolic LHCII translation in response to light quantity changes. In the green unicellular alga Chlamydomonas reinhardtii, the cytosolic RNA-binding protein NAB1 represses translation of certain LHCII isoform mRNAs. Specific nitrosylation of Cys-226 decreases NAB1 activity and could be demonstrated in vitro and in vivo. The less active, nitrosylated form of NAB1 is found in cells acclimated to limiting light supply, which permits accumulation of lightharvesting proteins and efficient light capture. In contrast, elevated light supply causes its denitrosylation, thereby activating the repression of light-harvesting protein synthesis, which is needed to control excitation pressure at photosystem II. Denitrosylation of recombinant NAB1 is efficiently performed by the cytosolic thioredoxin system in vitro. To our knowledge, NAB1 is the first example of stimulus-induced denitrosylation in the context of photosynthetic acclimation. By identifying this novel redox cross-talk pathway between chloroplast and cytosol, we add a new key element required for drawing a precise blue print of the regulatory network of light harvesting.

Nitric Oxide Mediates Nitrite-Sensing and Acclimation and Triggers a Remodeling of Lipids

“…Thus, our analysis could not lead us to identify any component acting in the synthesis of NO c besides NOA. Recently, NO c has been shown to nitrosylate an RNAbinding protein in the cytosol of Chlamydomonas, NAB1, which represses the translation of some mRNAs of photosynthetic components such as LHC II isoforms (Berger et al, 2016). A NAB1-like sequence was identified, lacking the nitrosylated domain identified in the Chlamydomonas sequence; nevertheless, the NAB1-like gene appeared as up-regulated by the treatment.…”

The soluble guanylate cyclase CYG12 is required for the acclimation to hypoxia and trophic regimes in Chlamydomonas reinhardtii

“…POR1 (coding for light‐dependent protochlorophyllide reductase) and the shorter splice variant of FLU , encoding a regulator of Chl biosynthesis (Falciatore et al ., ) were lower abundant also under standard growth conditions (Table ). Ten transcripts for light‐harvesting complex proteins as well as NAB1 , encoding an RNA‐binding protein that regulates the translation of several RNAs for LHCII proteins (Mussgnug et al ., ; Berger et al ., ) had 4‐ to 29‐fold lower amounts in the dark‐hypoxic CYG12 knockdown strain than in the wild‐type (Table and Data S1.5). It appeared that their lower amounts in the transformant resulted from two trends: First, all transcripts were less abundant already under standard growth conditions (0 h), although they fell below our cutoff.…”

“…reinhardtii can be S ‐nitrosylated, such as PSII and PSI subunits, LHC proteins and enzymes of Chl biosynthesis including POR1 (Morisse et al ., ). NAB1, a cytosolic protein that represses the translation of LHCBM mRNAs and whose transcript was also mis‐regulated in strain ami CYG12 (Table ), can be deactivated by S ‐nitrosylation (Berger et al ., ).…”

“…In most cases, the mode of action of the NO molecule is not known, however, post‐translational modification in form of S ‐nitrosylation exerts regulatory effects on C . reinhardtii proteins (Morisse et al ., ; Berger et al ., ). The best understood NO‐based signalling pathway in C .…”

“…In C . reinhardtii , NO has been proposed to be involved in several processes, too, such as the regulation of nitrate assimilation (de Montaigu et al ., ; Sanz‐Luque et al ., ), the regulated degradation of the cytochrome b 6 f complex upon nitrogen starvation (Wei et al ., ), acclimation to different light intensities (Berger et al ., ) and cell cycle progression (Pokora et al ., ). In most cases, the mode of action of the NO molecule is not known, however, post‐translational modification in form of S ‐nitrosylation exerts regulatory effects on C .…”