Effects of Arbuscular Mycorrhizal Fungi and Metal-Tolerant Pseudomonas fluorescens on Mitigating Cadmium and Zinc Stress in Tomato

Heavy metal (HM) contamination in agricultural soils poses a significant threat to soil health and plant productivity. This study investigates the impact of cadmium (Cd) and zinc (Zn) stress on tomato plants (Solanum lycopersicum) and explores the mitigation potential of microbial biostimulants (MBs), including arbuscular mycorrhizal fungi (AMF) and Pseudomonas fluorescens So_08 (PGPR), over a 52-day period using multi-omics approaches. Root exudate profiling revealed distinct metabolic changes under HM stress, which compromised soil–plant interactions. Cd stress reduced the secretion of phenylpropanoids (sum LogFC: −45.18), lipids (sum LogFC: −27.67), and isoprenoids (sum LogFC: −11–67), key metabolites in antioxidative defense, while also suppressing rhizosphere fungal populations. Conversely, Zn stress enhanced lipid exudation (such as sphingolipids and sterols, as sum LogFC of 8.72 and 9.99, respectively) to maintain membrane integrity and reshaped rhizobacterial communities. The MBs application mitigated HM-induced stress by enhancing specialized metabolite syntheses, including cinnamic acids, terpenoids, and flavonoids, which promoted crop resilience. MBs also reshaped microbial diversity, fostering beneficial species like Portibacter spp., Alkalitalea saponilacus under Cd stress, and stimulating rhizobacteria like Aggregatilinea spp. under Zn stress. Specifically, under Cd stress, bacterial diversity remained relatively stable, suggesting their resilience to Cd. However, fungal communities exhibited greater sensitivity, with a decline in diversity in Cd-treated soils and partial recovery when MBs were applied. Conversely, Zn stress caused decline in bacterial α-diversity, while fungal diversity was maintained, indicating that Zn acts as an ecological filter that suppresses sensitive bacterial taxa and favors Zn-tolerant fungal species. Multi-omics data integration combined with network analysis highlighted key features associated with improved nutrient availability and reduced HM toxicity under MB treatments, including metabolites and microbial taxa linked to sulfur cycling, nitrogen metabolism, and iron reduction pathways. These findings demonstrate that MBs can modulate plant metabolic responses and restore rhizosphere microbial communities under Cd and Zn stress, with PGPR showing broader metabolomic recovery effects and AMF influencing specific metabolite pathways. This study provides new insights into plant–microbe interactions in HM-contaminated environments, supporting the potential application of biostimulants for sustainable soil remediation and plant health improvement.