Genomic Surveillance of Epiphytic Pseudomonas syringae Highlights Shared Reservoirs and Cross-Habitat Threats to Cherry Orchards and Nearby Woodland Plants.

Plant surfaces host diverse microbial communities acting as reservoirs for pathogenic lineages, yet the ecological dynamics and evolutionary consequences of such reservoirs remain underexplored. We conducted landscape-scale genomic surveillance of Pseudomonas syringae on symptomless leaves of cultivated cherry in orchards and wild plant species in adjacent woodlands across the UK, aiming to understand how phyllosphere populations contribute to the emergence of bacterial canker. Whole genome sequencing of 540 isolates collected over two years and across four regions revealed 10 diverse P. syringae phylogroups (PGs) on symptomless leaves. Both orchard and woodland environments harboured a similar range of PGs, but recovery frequency was very different. PG2d strains dominated cherry orchards, whereas PGs 2b and 13a were prevalent in woodlands. Certain PG2d subclades, recovered from both environments, caused disease on cultivated and wild cherry leaves. Additional strains were found to be pathogenic to Phaseolus bean pods. The pathogens of cherry were characterised by the presence of genes encoding the synthesis of the pathotoxin syringolin A and a subset of effector proteins including HopAW1, AvrRpm1 and HopAR1. Resolution of subclades within PG2d provided insights into the emergence of virulent epiphytic strains that have not yet reached the mostly northerly sampling sites but are threats to both cultivated and environmental Prunus spp. Fine-scale analysis of subclade PG2d-3 revealed potential divergence between orchard and woodland populations, with 49 genes exclusive to a woodland lineage. Thirty-eight of these genes were found within prophages, indicating the potential role of bacteriophage-mediated horizontal gene transfer in adaptation to non-agricultural reservoirs.