Regulation of Metabolites, Gene Expression, and Antioxidant Enzymes to Environmentally Relevant Lead and Zinc in the Halophyte Suaeda salsa

As a pioneer halophyte, Suaeda salsa can grow in the intertidal zones, which are often polluted by heavy metals from both terrigenous wastewater and tidewater containing high concentrations of heavy metals. Therefore S. salsa is potentially suitable as a biomonitor for heavy-metal pollution in the intertidal zones. In this study, regulation of metabolites, gene expression, and antioxidant status of environmentally relevant lead and zinc were characterized using NMR-based metabolomics, real-time quantitative reverse transcription polymerase chain reaction, and antioxidant enzyme activities. In Pb-exposed S. salsa samples, only decreased tyrosine was observed, with statistical significance approaching 0.05. Metabolic biomarkers in Zn-exposed S. salsa samples included increased amino acids (valine, isoleucine, leucine, threonine, asparagine, and phenylalanine), and decreased acetate, glucose, ferulate, and fumarate. Increased succinate, aspartate, and malonate and decreased fructose were uniquely found in mixed Pb- and Zn-exposed samples in addition to the similar metabolic changes such as alanine, glucose, fumarate, and ferulate in Zn-exposed samples. Based on the metabolic biomarkers, gene expressions, and antioxidant enzyme activities, both Zn and mixed Pb and Zn induced significant oxidative stress and disturbances in energy metabolism, photosynthesis/glucogenesis, and protein biodegradation in S. salsa. However, environmentally relevant Pb could induce slight oxidative stress in S. salsa as indicated by increased catalase gene expression levels and catalase activities.