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Ultraviolet (UV) A radiation (315–400 nm) is the predominant component of solar UV radiation that reaches the Earth’s surface. However, the underlying mechanisms of the positive effects of UV-A on photosynthetic organisms have not yet been elucidated. In this study, we investigated the effects of UV-A radiation on the growth, photosynthetic ability, and metabolome of the edible cyanobacterium Nostoc sphaeroides. Exposures to 5–15 W m−2 (15–46 µmol photons m−2 s−1) UV-A and 4.35 W m−2 (20 μmol photons m−2 s−1) visible light for 16 days significantly increased the growth rate and biomass production of N. sphaeroides cells by 18%–30% and 15%–56%, respectively, compared to the non-UV-A-acclimated cells. Additionally, the UV-A-acclimated cells exhibited a 1.8-fold increase in the cellular nicotinamide adenine dinucleotide phosphate (NADP) pool with an increase in photosynthetic capacity (58%), photosynthetic efficiency (24%), QA re-oxidation, photosystem I abundance, and cyclic electron flow (87%), which further led to an increase in light-induced NADPH generation (31%) and ATP content (83%). Moreover, the UV-A-acclimated cells showed a 2.3-fold increase in ribulose-1,5-bisphosphate carboxylase/oxygenase activity, indicating an increase in their carbon-fixing capacity. Gas chromatography–mass spectrometry-based metabolomics further revealed that UV-A radiation upregulated the energy-storing carbon metabolism, as evidenced by the enhanced accumulation of sugars, fatty acids, and citrate in the UV-A-acclimated cells. Therefore, our results demonstrate that UV-A radiation enhances energy flow and carbon assimilation in the cyanobacterium N. sphaeroides. IMPORTANCE Ultraviolet (UV) radiation exerts harmful effects on photo-autotrophs; however, several studies demonstrated the positive effects of UV radiation, especially UV-A radiation (315–400 nm), on primary productivity. Therefore, understanding the underlying mechanisms associated with the promotive effects of UV-A radiation on primary productivity can facilitate the application of UV-A for CO2 sequestration and lead to the advancement of photobiological sciences. In this study, we used the cyanobacterium Nostoc sphaeroides, which has an over 1,700-year history of human use as food and medicine, to explore its photosynthetic acclimation response to UV-A radiation. As per our knowledge, this is the first study to demonstrate that UV-A radiation increases the biomass yield of N. sphaeroides by enhancing energy flow and carbon assimilation. Our findings provide novel insights into UV-A-mediated photosynthetic acclimation and provide a scientific basis for the application of UV-A radiation for optimizing light absorption capacity and enhancing CO2 sequestration in the frame of a future CO2 neutral, circular, and sustainable bioeconomy. [ABSTRACT FROM AUTHOR]

Cyanobacteria are important players in the global carbon cycle, accounting for approximately 25% of global CO2 fixation. Their CO2-concentrating mechanisms (CCMs) are thought to play a key role in cyanobacterial calcification, but the mechanisms are not completely understood. In Synechocystis sp. strain PCC 6803, a single Ca2+/H+ exchanger (Slr1336) controls the Ca2+/H+ exchange reaction. We knocked out the exchanger and investigated the effects on cyanobacterial calcification and CCMs. Inactivation of slr1336 significantly increased the calcification rate and decreased the zeta potential, indicating a relatively stronger Ca2+-binding ability. Some genes encoding CCM-related components showed increased expression levels, including the cmpA gene, which encodes the Ca2+-dependent HCO3- transporter BCT1. The transcript level of cmpA in the mutant was 30 times that in wild type. A Western blot analysis further confirmed that protein levels of CmpA were higher in the mutant than the wild type. Measurements of inorganic carbon fluxes and O2 evolution proved that both the net HCO3- uptake rate and the BCT1 transporter supported photosynthetic rate in the slr1336 mutant were significantly higher than in the wild type. This would cause the mutant cells to liberate more OH- ions out of the cell and stimulate CaCO3 precipitation in the microenvironment. We conclude that the mutation of the Ca2+/H+ exchanger in Synechocystis promoted the cyanobacterial calcification process by upregulating CCMs, especially the BCT1 HCO3- transporter. These results shed new light on the mechanism by which CCM-facilitated photosynthesis promotes cyanobacterial calcification. [ABSTRACT FROM AUTHOR]