Metallomics and NMR-based metabolomics of Chlorella sp. reveal the synergistic role of copper and cadmium in multi-metal toxicity and oxidative stress

Metallomics. 2015 Mar;7(3):426-38. doi: 10.1039/c4mt00253a.

Abstract

Industrial wastewaters often contain high levels of metal mixtures, in which metal mixtures may have synergistic or antagonistic effects on aquatic organisms. A combination of metallomics and nuclear magnetic resonance spectroscopy (NMR)-based metabolomics was employed to understand the consequences of multi-metal systems (Cu, Cd, Pb) on freshwater microalgae. Morphological characterization, cell viability and chlorophyll a determination of metal-spiked Chlorella sp. suggested synergistic effects of Cu and Cd on growth inhibition and toxicity. While Pb has no apparent effect on Chlorella sp. metabolome, a substantial decrease of sucrose, amino acid content and glycerophospholipid precursors in Cu-spiked microalgae revealed Cu-induced oxidative stress. Addition of Cd to Cu-spiked cultures induced more drastic metabolic perturbations, hence we confirmed that Cu and Cd synergistically influenced photosynthesis inhibition, oxidative stress and membrane degradation. Total elemental analysis revealed a significant decrease in K, and an increase in Na, Mg, Zn and Mn concentrations in Cu-spiked cultures. This indicated that Cu is more toxic to Chlorella sp. as compared to Cd or Pb, and the combination of Cu and Cd has a strong synergistic effect on Chlorella sp. oxidative stress induction. Oxidative stress is confirmed by liquid chromatography tandem mass spectrometry analysis, which demonstrated a drastic decrease in the GSH/GSSG ratio solely in Cu-spiked cultures. Interestingly, we observed Cu-facilitated Cd and Pb bioconcentration in Chlorella sp. The absence of phytochelatins and an increment of extracellular polymeric substances (EPS) yields in Cu-spiked cultures suggested that the mode of bioconcentration of Cd and Pb is through adsorption of free metals onto the algal EPS rather than intracellular chelation to phytochelatins.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Biomass
  • Biopolymers / metabolism
  • Cadmium / toxicity*
  • Chlorella / cytology
  • Chlorella / drug effects
  • Chlorella / growth & development
  • Chlorella / metabolism*
  • Chlorophyll / metabolism
  • Chlorophyll A
  • Copper / toxicity*
  • Magnetic Resonance Spectroscopy
  • Metabolome / drug effects
  • Metabolomics*
  • Oxidative Stress / drug effects*
  • Peptides / metabolism
  • Principal Component Analysis
  • Proton Magnetic Resonance Spectroscopy
  • Sulfhydryl Compounds / metabolism
  • Time Factors

Substances

  • Biopolymers
  • Peptides
  • Sulfhydryl Compounds
  • Cadmium
  • Chlorophyll
  • Copper
  • Chlorophyll A