Microbial Alliances: Unveiling the Effects of a Bacterial and Fungal Cross-Kingdom SynCom on Bacterial Dynamics, Rhizosphere Metabolites, and Soybean Resilience in Acidic Soils

Acidic soils, covering 40 to 50% of arable land, hinder productivity due to phosphorus limitation and aluminum toxicity. Using a synthetic community (SynCom) approach, we tested a native <i>Rhizobium</i> (Rh) and a non-native <i>Ensifer fredii</i> (Ef) strain, both combined with the mycorrhizal fungus <i>Rhizophagus intraradices</i> (Ri), on soybean growth in acidic soil. The native RhRi SynCom outperformed EfRi, significantly improving soybean growth, yield, and soil health. Metagenomics and metabolomics revealed that RhRi significantly enhanced beneficial microorganisms (<i>AD3, Gemmataceae</i>) and metabolites (putrescine, stearic acid), hence improving nutrient cycling, stress tolerance, and membrane integrity. RhRi also enhanced soil enzyme activity (urease, phosphatases), which resulted in an increase in nitrogen and phosphorus availability and a decrease in rhizosphere toxicity. These alterations enhanced plant resilience, soil structure, and microbial diversity. RhRi activated metabolic pathways (amino acids, lipids, ABC transporters, and secondary metabolites) that are involved in nutrient acquisition and stress response. Conversely, EfRi provided minimal advantages, emphasizing the significance of native microbial compatibility. Our findings show that native SynComs boost crop resilience and production in acidic soils through synergistic microbial interactions and metabolic reprogramming, thereby offering a sustainable agricultural strategy in harsh environments.