Differential long-term tolerance to copper and salt stress by Bruguiera gymnorhiza and Kandelia obovata is driven by species-specific metabolic modulation and rhizobacterial recruitment

Abstract

The resilience of the plant phytobiome to environmental stress hinges on multitrophic interactions. This study reveals how Bruguiera gymnorhiza L. savigny and Kandelia obovata Sheue & al achieve differential tolerance to copper (Cu) toxicity and salt stress through distinct rhizobacterial recruitment and root metabolic modulation strategies. Using multiomics and chemical approaches, we analyzed rhizobacterial community dynamics, root/rhizosphere metabolic profiles, root/leaf antioxidant enzyme activities, and rhizosphere physicochemical properties. The results revealed that metabolic modulation was the primary stress response mechanism, especially in the less tolerant B. gymnorhiza. Based on the number of differentially abundant metabolites, lipids and lipid-like molecules dominated stress response in both the roots and rhizospheres, except in the roots of K. obovata, where phenylpropanoids and polyketides dominated. The marked differences observed in eicosanoid metabolism between the roots and rhizospheres highlight how species-specific adjustments determine stress tolerance levels. These distinct metabolic strategies influenced species-specific rhizobacterial recruitment, optimizing nutrient uptake and growth. Specifically, K. obovata exhibited more effective enrichment of stress-tolerant rhizobacteria (e.g., Bacteroidota, Firmicutes, and Proteobacteria), which was correlated with improved tolerance under all stresses and improved growth under Cu and Cu-salt stress. In contrast, B. gymnorhiza relies on the synergistic effect of Cu-salt stress to recruit beneficial consortia (Proteobacteria) for 11.5% growth promotion. Thus, tolerance to Cu/salt stress relies on species-specific microbiome-metabolite cross-talk, with the inherent adaptability of K. obovata outperforming the stress-dependent responses of B. gymnorhiza. These findings underscore microbiome-assisted restoration following species-specific management strategies.