Multi-leveled insights into the response of the eelgrass Zostera marina L to Cu than Cd exposure

Abstract

Seagrass beds are recognized as critical and among the most vulnerable habitats on the planet; seagrass colonize the coastal waters where heavy metal pollution is a serious problem. In this study, the toxic effects of copper and cadmium in the eelgrass Zostera marina L. were observed at the individual, subcellular, physiologically biochemical, and molecular levels. Both Cu and Cd stress significantly inhibited the growth and the maximal quantum yield of photosystem II (Fv/Fm); and high temperature increased the degree of heavy metal damage, while low temperatures inhibited damage. The half-effect concentration (EC50) of eelgrass was 28.9 μM for Cu and 2246.8 μM for Cd, indicating Cu was much more toxic to eelgrass than Cd. The effect of Cu and Cd on photosynthesis was synergistic. After 14 days of enrichment, the concentration of Cu in leaves and roots of Z. marina was 48 and 37 times higher than that in leaf sheath, and 14 and 11 times higher than that in rhizome; and the order of Cd concentration in the organs was root > leaf > rhizome > sheath. Heavy metal uptake mainly occurred in the organelles, and Cd enrichment also occurred to a certain extent in the cytoplasm. Transcriptome results showed that a number of photosynthesis-related KEGG enrichment pathways and GO terms were significantly down-regulated under Cd stress, suggesting that the photosynthetic system of eelgrass was severely damaged at the transcriptome level, which was consistent with the significant inhibition of Fv/Fm and leaf yellowing. Under Cu stress, the genes related to glutathione metabolic pathway were significantly up-regulated, together with the increased autioxidant enzyme activity of GSH-PX. In addition, the results of recovery experiment indicated that the damage caused by short-term Cd and Cu stress under EC50 was reversible. These results provide heavy metal toxic effects at multiple levels and information relating to the heavy metal resistance strategies evolved by Z. marina to absorb and isolate heavy metals, and highlight the phytoremediation potential of this species especially for Cd.