Unveiling the compatibility of the interaction between Bacillus velezensis and Rhizophagus irregularis

Abstract

Context. Nowadays, one of the most promising eco-friendly alternatives to the use of chemical pesticides and fertilizers for plant health management is the use of beneficial microorganisms. Several species of plant growth promoting rhizobacteria (PGPR) and arbuscular mycorrhizal fungi (AMF) are currently commercially available in this context. PGPR and AMF used individually have shown significant improvements in various field crops. Evidence has also accumulated on their synergistic interactions for plant development. However, how PGPR interact with AMF have not yet been elucidated. The PGPR, Bacillus velezensis, and the AMF, Rhizophagus irregularis, are model microorganisms respectively for bioprotection and biofertilization of plants. Their interaction has never been studied but can lead to a potential synergistic cooperation against plant pathogens. However, B. velezensis has the potential to produce a wide range of bioactive secondary metabolites (BSMs) including antifungal compounds which can therefore inhibit the R. irregularis growth and survival. Objectives. The purpose of this study is to provide evidence that B. velezensis GA1 and R. irregularis MUCL 41833 can evolve together without prejudice to either partner. Subsequently, to investigate the potential modulation of BSMs produced by the bacterium in the context of the hyphosphere. Methods. Live cell microscopy imaging in vivo was performed using a more innovative technique to follow B. velezensis colonization along AMF hyphae and to evaluate the R. irregularis vitality during the interaction. The bacilli biofilm formation was also investigated by RT-qPCR analysis. The viability of the fungi was analysed by histochemical staining. Based on the evidence of their compatible interaction, molecular level experiments were performed to further understand their interaction. The analysis of the B. velezensis metabolome produced in mycorrhiza was achieved by LC-MS as well as the analysis of the lipopeptidome by RT-qPCR. By an indirect approach, the B. velezensis growth was also tested in hyphal exudates compared in root exudates mimicking (RE) medium. The B. velezensis lipopeptidome produced in hyphal exudates and in RE was analysed by LC-MS. Results. We have unveiled the compatibility of the interaction between B. velezensis and R. irregularis. B. velezensis colonizes along R. irregularis hyphae without impacting vitality and viability of its host. We further supported that their interaction is due to the modulation of BSMs produced by B. velezensis in the context of the hyphosphere. We also identified that this filtering effect of the AMF on the GA1 metabolome was performed by its exudates. Conclusions. This study provides new insights of crosstalk establish between beneficial microorganisms that may occur in the rhizosphere. Thus, this work highlights the potential use of microbial consortia that can lead to additive or synergistic results to promote plant growth and health for the future of sustainable agriculture.