Bacteria-phage coevolution drives variation in bacterial wilt disease incidence via resistance-virulence trade-offs

Bacteria-phage coevolution often results in correlated fitness effects on partner species. Whether coevolutionary changes impact the ecology of the surrounding communities is unclear. Here we link coevolution between the phytopathogenic bacterium Ralstonia pseudosolanacearum and its phage parasites to bacterial wilt disease patterns across four geographically disconnected tomato fields. We find that bacteria and phages are locally adapted between and within fields. Phage infectivity was highest on sympatric bacteria, and bacteria showed greater phage resistance when isolated from healthy than diseased plants. The modularity of phage-bacteria coevolution was associated with field-specific anti-phage defence system patterns and locally adapted phage populations. Moreover, phages selected for field-specific mutations in different phage receptor genes, which were negatively associated with virulence measured in planta, suggesting why phage-resistant but weakly virulent pathogen isolates are associated with healthy tomato plants within fields. Our findings show that bacteria-phage coevolution results in patchy plant disease distribution through phage resistance-virulence trade-offs.