Nitric Oxide Remodels the Photosynthetic Apparatus upon S-Starvation in Chlamydomonas reinhardtii

Many photosynthetic autotrophs have evolved responses that adjust their metabolism to limitations in nutrient availability. Here we report a detailed characterization of the remodeling of photosynthesis upon sulfur starvation under heterotrophy and photo-autotrophy in the green alga (Chlamydomonas reinhardtii). Photosynthetic inactivation under low light and darkness is achieved through specific degradation of Rubisco and cytochrome b₆f and occurs only in the presence of reduced carbon in the medium. The process is likely regulated by nitric oxide (NO), which is produced 24 h after the onset of starvation, as detected with NO sensitive fluorescence probes visualized by fluorescence microscopy. We provide pharmacological evidence that intracellular NO levels govern this degradation pathway: the addition of a NO scavenger decreases the rate of cytochrome b₆f and Rubisco degradation, whereas NO donors accelerate the degradation. Based on our analysis of the relative contribution of the different NO synthesis pathways, we conclude that the NO₂-dependent nitrate reductase-independent pathway is crucial for NO production under sulfur starvation. Our data argue for an active role for NO in the remodeling of thylakoid protein complexes upon sulfur starvation.