Ralstonia solanacearum Facing Spread-Determining Climatic Temperatures, Sustained Starvation, and Naturally Induced Resuscitation of Viable but Non-Culturable Cells in Environmental Water

Ralstonia solanacearum is a bacterial phytopathogen affecting staple crops, originally from tropical and subtropical areas, whose ability to survive in temperate environments is of concern under global warming. In this study, two R. solanacearum strains from either cold or warm habitats were stressed by simultaneous exposure to natural oligotrophy at low (4 °C), temperate (14 °C), or warm (24 °C) temperatures in environmental water. At 4 °C, the effect of temperature was higher than that of oligotrophy, since R. solanacearum went into a viable but non-culturable (VBNC) state, which proved to be dependent on water nutrient contents. Resuscitation was demonstrated in vitro and in planta. At 14 °C and 24 °C, the effect of oligotrophy was higher than that of temperature on R. solanacearum populations, displaying starvation-survival responses and morphological changes which were stronger at 24 °C. In tomato plants, starved, cold-induced VBNC, and/or resuscitated cells maintained virulence. The strains behaved similarly regardless of their cold or warm areas of origin. This work firstly describes the natural nutrient availability of environmental water favoring R. solanacearum survival, adaptations, and resuscitation in conditions that can be found in natural settings. These findings will contribute to anticipate the ability of R. solanacearum to spread, establish, and induce disease in new geographical and climatic areas.