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Low Concentrations of Silver Nanoparticles and Silver Ions Perturb the Antioxidant Defense System and Nitrogen Metabolism in N2-Fixing Cyanobacteria.

Although toxic effects of silver nanoparticles (AgNPs) on aquatic organisms have been extensively reported, responses of nitrogen-fixing cyanobacteria to AgNPs/Ag+ under environmentally relevant concentrations are largely unknown. Here, cyanobacteria were exposed to different concentrations of AgNPs (0.01, 0.1, and 1 mg/L) or Ag+ (0.1, 1, and 10 μg/L) for 96 h. The impacts of AgNPs and Ag+ on photosynthesis and N2 fixation in cyanobacteria (Nostoc sphaeroides) were evaluated. In addition, gas chromatography-mass spectrometry (GC-MS)-based metabolomics was employed to give an instantaneous snapshot of the physiological status of the cells under AgNP/Ag+ exposure. Exposure to high doses of AgNPs (1 mg/L) or Ag+ (10 μg/L) caused growth inhibition, reactive oxygen species overproduction, malondialdehyde accumulation, and decreased N2 fixation. In contrast, low doses of AgNPs (0.01 and 0.1 mg/L) and Ag+ (0.1 and 1 μg/L) did not induce observable responses. However, metabolomics revealed that metabolic reprogramming occurred even at low concentrations of AgNP and Ag+ exposure. Levels of a number of antioxidant defense-related metabolites, especially phenolic acid and polyphenols (gallic acid, resveratrol, isochlorogenic acid, chlorogenic acid, cinnamic acid, 3-hydroxybenzoic acid, epicatechin, catechin, and ferulic acid), significantly decreased in response to AgNPs or Ag+. This indicates that AgNPs and Ag+ can disrupt the antioxidant defense system and disturb nitrogen metabolism even at low-dose exposure. Metabolomics was shown to be a powerful tool to detect "invisible" changes, not observable by typical phenotypic-based endpoints.