Abstract

Silver nanoparticles (AgNPs) are one of the most used engineered nanomaterials. Despite progress in assessing their environmental implications, knowledge gaps exist concerning the metabolic perturbations induced by AgNPs on phytoplankton, essential organisms in global biogeochemical cycles and food-web dynamics. We combine targeted metabolomics, biouptake and physiological response studies to elucidate metabolic perturbations in alga Poterioochromonas malhamensis induced by AgNPs and dissolved Ag. We show time-dependent perturbation of the metabolism of amino acids, nucleotides, fatty acids, tricarboxylic acids, photosynthesis and photorespiration by both Ag-treatments. The results suggest that dissolved Ag ions released by AgNPs are the major toxicity driver; however, AgNPs internalized in food vacuoles contributed to the perturbation of amino acid metabolism, TCA cycle and oxidative stress. The metabolic perturbations corroborate the observed physiological responses. We highlight the potential of metabolomics as a tool for understanding the molecular basis for these metabolic and physiological changes, and for early detection of stress.

Highlights

  • Metabolomics tracks the changes in low-molecular-weight metabolites involved in different biological ­reactions[1,2] under different environmental stimuli and stressors

  • The present study for the first time revealed the metabolic perturbations induced by AgNPs following their uptake and accumulation in the food vacuoles of golden-brown alga P. malhamensis

  • Results of targeted metabolomics demonstrated that the exposure to AgNPs and dissolved Ag resulted in time-dependent perturbation of the concentration of metabolites involved in various metabolic pathways involving amino acids, nucleotides, fatty acids, tricarboxylic acid (TCA), antioxidants, photosynthesis and photorespiration

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Summary

Introduction

Metabolomics tracks the changes in low-molecular-weight metabolites involved in different biological ­reactions[1,2] under different environmental stimuli and stressors. Nanoparticle-induced metabolic perturbations to environmentally relevant organisms, such as plants, have only been recently studied systematically by both untargeted and targeted ­metabolomics[4,5,6,7,8,9]. While it is useful to study the physiological responses of AgNPs, there is a need to understand how AgNPs affect the metabolic processes of these organisms. We examine the interactions of citrate-coated 20 nm AgNPs with the freshwater alga Poterioochromonas malhamensis, as representative of freshwater phytoplankton. P. malhamensis uses a wide selection of different organic food sources via phagotrophy or ­osmotrophy[29]. We assume this alga can take up AgNPs and their aggregates via phagocytosis. The results highlight the high added value of metabolomics to elucidate the mechanisms that cause the physiological response in phytoplankton induced by stressors such as engineered nanomaterials

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