Low Concentrations of Silver Nanoparticles and Silver Ions Perturb the Antioxidant Defense System and Nitrogen Metabolism in N-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 N fixation in cyanobacteria () 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 N 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.