Phyllosphere microbiome shifts reveal Gluconobacter japonicus T12B as a biocontrol agent against Xanthomonas in tomato through genomic and functional characterization

AIMS: Bacterial spot disease caused by Xanthomonas spp. is a major threat to tomato production that leads to significant yield losses. As these pathogens invade through stomata and wounds, understanding the phyllosphere microbiome dynamics during infection is critical for identifying potential biocontrol agents. In this study, we profiled the tomato phyllosphere microbiome shift during Xanthomonas infection, assessed the antagonistic activity of a phyllosphere bacterium, and characterized its genetic features through whole genome analysis. METHODS AND RESULTS: Phyllosphere microbiome analysis was performed on control and Xanthomonas-infected tomato plants using the leaf swabbing method and 16S rRNA gene amplicon sequencing with various primer sets. A significant increase in the abundance of Acetobacteraceae in infected plants prompted the targeted cultivation of the taxon, which subsequently led to the isolation of strain T12B. It exhibited strong in vitro and in vivo antagonistic activity against Xanthomonas, primarily through organic acid production. Whole genome analysis confirmed T12B as Gluconobacter japonicus subsp. japonicus. The genome of T12B encodes 2792 coding DNA sequences, including complete pathways for acetic, gluconic, and ketogluconic acid biosynthesis, as well as other putative genes that may contribute to its antagonistic activity against Xanthomonas. CONCLUSIONS: Tomato phyllosphere microbiome profiling facilitated the targeted isolation of G. japonicus T12B that demonstrated potential for disease suppression and biocontrol applications in tomato.