Synthetic phyllosphere microbiota enhance wax gourd plant growth and suppress Phytophthora capsici by reshaping microbial communities

The role of rhizosphere microbes in suppressing plant diseases is well-studied, but the response of phyllosphere microbes to disease invasion remains largely unexplored. In this study, we isolated biocontrol and plant growth-promoting bacterial strains from leaves of the wax gourd plant. In vitro tests on 63 bacterial strains revealed that 15, 11, and 12 strains produced amylases, cellulases, and proteases, respectively. Moreover, 14 strains solubilized organic phosphates, 13 inorganic phosphorus, and 3 showed high indole-3-acetic acid production. Five strains exhibited strong antifungal activity against Fusarium graminearum , F. equisetum , F. oxysporum , Colletotrichum capsici , Coccidioides phaseolus , and Phytophthora capsici . The five wax gourd leaf strains, along with the previously isolated Bacillus thuringiensis GBAC46, were used to construct four synthetic microbial communities (SynComs: A, B, C, and D). These five strains were selected based on their antagonistic activity and their capacities to produce extracellular enzymes, synthesize growth-promoting hormones, and solubilize phosphate. SynCom A showed reduced swarming motility and thinner biofilms, while SynComs B, C, and D displayed higher motility and well-structured, uniform biofilms. Additionally, the crude SynCom extracts markedly inhibited P. capsici growth. SynComs B and D produced surfactins, fengycins, and iturins, whereas SynComs A and C generated only surfactins and iturins. Notably, SynCom B showed elevated fengycin production associated with strong antimicrobial activity. In pot experiments, SynCom B significantly enhanced plant growth, increasing root and shoot length, fresh and dry weight, and stem diameter compared with the control. All four SynComs reduced the disease index compared to the control, with SynCom B showing the highest efficacy (40.48 %) against P. capsici by modulating defense genes ERF1 and EIN3 . In the presence of P. capsici , SynComs reshaped bacterial communities, such as Shannon, Simpson, and Inv_simpson diversity, enriching beneficial genera like Bacillus , Delftia , and Pseudomonas in the wax gourd phyllosphere. These findings reveal novel mechanisms of SynCom-mediated leaf blight suppression, supporting its potential as a biopesticide.