Proximity-based defensive mutualism between Streptomyces and Mesorhizobium by sharing and sequestering iron

Abstract

Microorganisms living in soil maintain intricate interactions among themselves, forming the soil microbiota that influences the rhizosphere microbiome and plant growth. However, the mechanisms underlying the soil microbial interactions remain unclear. Streptomyces and Mesorhizobium are commonly found in soil and serve as plant growth-promoting rhizobacteria (PGPR). Here, we identified an unprecedented interaction between the colonies of red-soil-derived Streptomyces sp. FXJ1.4098 and Mesorhizobium sp. BAC0120 and referred to it as “proximity-based defensive mutualism (PBDM)”. We found that metabolite-mediated iron competition and sharing between the two microorganisms was responsible for PBDM. S. sp. FXJ1.4098 produced a highly diffusible siderophore, desferrioxamine (DFO), which made iron unavailable to co-cultured M. sp. BAC0120, thereby inhibiting its growth. S. sp. FXJ1.4098 also released poorly diffusible iron-porphyrin complexes, which could be utilized by M. sp. BAC0120, thereby restoring the growth of nearby M. sp. BAC0120. Furthermore, in ternary interactions, the PBDM strategy contributed to the protection of M. sp. BAC0120 close to S. sp. FXJ1.4098 from other microbial competitors, resulting in the coexistence of these two PGPR. A scale-up pairwise interaction screening suggested that the PBDM strategy may be common between Mesorhizobium and red-soil-derived Streptomyces. These results demonstrate the key role of iron in complex microbial interactions and provide novel insights into the coexistence of PGPR in soil.