Physiological and metagenomic strategies uncover the rhizosphere bacterial microbiome succession underlying three common environmental stresses in cassava

Highlights: • Cd, glyphosate and tetracycline inhibit cassava growth and redox homeostasis. • Rhizosphere microbiome bacterial succession responded to stresses is revealed. • Stresses derived oxidative damage through rhizosphere microbiome succession. • Phyllosphere transplantation could alleviate stresses triggered toxic effect. The most common environmental pollutants such as cadmium (Cd), glyphosate and tetracycline have led to profoundly adverse impacts on plant productivity. However, how tropical crops such as cassava sense these pollutants via roots and how rhizosphere microbiome interacts with the host and pollutants remain largely unknown. In this study, we found these stresses significantly inhibited plant growth and triggered cell damage in a dosage-dependent manner, and the toxic effect on redox homeostasis was correlated with antioxidant metabolism. Using metagenomics technique, we found the rhizosphere microbiomes dynamically altered as the dose of these stresses increased. We also identified stressor-associated metagenome-assembled genomes and microbial metabolic pathways as well as mobile genetic elements in the rhizosphere microbiomes. Next, a co-occurrence network of both physiological and microbiome features was constructed to explore how these pollutants derived oxidative damage through the microbiome succession. Notably, phyllosphere transplantation of Agrobacterium tumefaciens or Pseudomonas stutzeri can significantly alleviate the negative effects of stresses on cassava growth and redox homeostasis. Collectively, this study demonstrated the dynamics of rhizosphere bacterial microbiome of cassava under three common environmental stresses, and A. tumefaciens and P. stutzeri could be developed as potential beneficial bacteria to alleviate Cd, glyphosate and tetracycline-triggered damage to cassava.