Interactions between pyrene and heavy metals and their fates in a soil-maize (Zea mays L.) system: Perspectives from the root physiological functions and rhizosphere microbial community

Highlights: • Pyrene-Cu/Cd co-presence influenced their degradation and accumulation in maize. • Co-contamination at low level enhanced metal extraction and pyrene degradation. • Cu stress (1000 mg/kg) reduced abundance of Mycobacterium and pyrene degradation. • Pyrene (≥400 mg/kg) influenced root metabolism and decreased metal extraction. • Cu showed an advantage in the competitive absorption and translocation with Cd. The co-occurrence of polycyclic aromatic hydrocarbons (PAHs) and heavy metals in agricultural soils has become a worldwide food crop security concern. Pot experiments, rhizosphere microbial metagenomic sequencing, and root metatranscriptomic sequencing were performed to investigate the interactions among pyrene, Cu, and Cd in a soil-maize (Zea mays L.) system. This study provided direct evidence that the co-presence of PAHs and heavy metals changed the root physiological functions and the rhizosphere microbial community, which subsequently influenced the fate of the contaminants. Co-contamination at low levels tended to enhance the uptake potential and biodegradation performance of the plant, whereas increased contaminant concentrations produced opposite effects. The co-presence of 1000 mg/kg Cu decreased the abundance of Mycobacterium in the rhizosphere and reduced pyrene degradation by 12%–16%. The presence of 400–750 mg/kg pyrene altered the metabolic processes, molecular binding functions, and catalytic activity of enzymes in the maize roots, thus impeding the phytoextraction of Cu and Cd. Competitive absorption between Cu and Cd was observed for the 800–1000 mg/kg Cu and 50–100 mg/kg Cd co-treatment, in which Cu showed a competitive advantage, enhancing its root-to-shoot translocation. These findings provide important information for the production of safe crops and for the development of phytoremediation technologies.