Photosynthetic organisms support cell metabolism by harvesting sunlight to fuel the photosynthetic electron transport. The flow of excitation energy and electrons in the photosynthetic apparatus needs to be continuously modulated to respond to dynamics of environmental conditions, and Flavodiiron (FLV) proteins are seminal components of this regulatory machinery in cyanobacteria. FLVs were lost during evolution by flowering plants, but are still present in nonvascular plants such as Physcomitrella patens. We generated P. patens mutants depleted in FLV proteins, showing their function as an electron sink downstream of photosystem I for the first seconds after a change in light intensity. flv knock-out plants showed impaired growth and photosystem I photoinhibition when exposed to fluctuating light, demonstrating FLV's biological role as a safety valve from excess electrons on illumination changes. The lack of FLVs was partially compensated for by an increased cyclic electron transport, suggesting that in flowering plants, the FLV's role was taken by other alternative electron routes.ife on Earth depends on oxygenic photosynthesis, which enables plants, algae, and cyanobacteria to convert light into chemical energy. Sunlight powers the transfer of electrons from water to NADP + by the activity of two photosystems (PS), PSII and PSI, thus generating NADPH and ATP to sustain cell metabolism. Natural environmental conditions are highly variable, and sudden changes in irradiation can drastically affect the flow of excitation energy and electrons. At the same time, the ATP and NADPH consumption rate is also highly dynamic because of a continuous metabolic regulation (1-3). Photosynthetic organisms evolved several mechanisms to modulate the flow of excitation energy and electrons according to metabolic constraints, diverting/ feeding electrons from/to the linear transport chain (3). These pathways modulate the ATP/NADPH ratio, as in the cyclic electron transport (CET) around PSI, where electrons are redirected from PSI to plastoquinone (PQ) or Cytb 6 f (4), contributing to proton translocation and ATP synthesis, but not to NADPH formation (5-9).In cyanobacteria, the Flavodiiron proteins (known as FLV) have been identified as an additional component of electron transport chain (10-12). FLV proteins are constituted by three distinct domains: a N-terminal β-lactamase-like domain, a flavodoxin-like domain, and a C-terminal NAD(P)H-flavin reductase-like domain. The former two domains are also found in FLV proteins from archaea and anaerobic bacteria, where they are involved in O 2 or NO reduction, whereas the latter is typical only of FLVs from oxygenic photosynthetic organisms (11-13). Recent studies showed that in cyanobacteria, the FLV1/FLV3 heterodimer catalyzes the light-dependent reduction of O 2 to water, using NADPH as electron donor (10, 11), protecting PSI from light stress (10). Another FLVs heterodimer, FLV2/FLV4, instead, has been shown to be active in photo-protection of PSII (14-16). FLVs also were found expre...

The seawater microalga Nannochloropsis gaditana is capable of accumulating a large fraction of reduced carbon as lipids. To clarify the molecular bases of this metabolic feature, we investigated light-driven lipid biosynthesis in Nannochloropsis gaditana cultures combining the analysis of photosynthetic functionality with transcriptomic, lipidomic and metabolomic approaches. Light-dependent alterations are observed in amino acid, isoprenoid, nucleic acid, and vitamin biosynthesis, suggesting a deep remodeling in the microalgal metabolism triggered by photoadaptation. In particular, high light intensity is shown to affect lipid biosynthesis, inducing the accumulation of diacylglyceryl-N,N,N-trimethylhomo-Ser and triacylglycerols, together with the up-regulation of genes involved in their biosynthesis. Chloroplast polar lipids are instead decreased. This situation correlates with the induction of genes coding for a putative cytosolic fatty acid synthase of type 1 (FAS1) and polyketide synthase (PKS) and the down-regulation of the chloroplast fatty acid synthase of type 2 (FAS2). Lipid accumulation is accompanied by the regulation of triose phosphate/inorganic phosphate transport across the chloroplast membranes, tuning the carbon metabolic allocation between cell compartments, favoring the cytoplasm, mitochondrion, and endoplasmic reticulum at the expense of the chloroplast. These results highlight the high flexibility of lipid biosynthesis in N. gaditana and lay the foundations for a hypothetical mechanism of regulation of primary carbon partitioning by controlling metabolite allocation at the subcellular level.