Temporal Dynamics of Eucalyptus Bacterial Wilt Covary Chronologically with Structural Shifts in Xylem-Endophytic Microbial Communities during Disease Progression

Eucalyptus bacterial wilt, caused by the Ralstonia solanacearum species complex (RSSC), is characterized by sudden and destructive outbreaks. Field epidemiological surveys revealed that the disease outbreak exhibits distinct temporal patterns, progressing from low-level accumulation to rapid spread over the years, with the core period of annual outbreak occurring from late August to early October. The pathogen colonized the entire tree at an early stage of disease development. The abundance and spatial distribution of the pathogen in the soil around infected trees exhibit a phased pattern: low and uniform abundance in the early stage, sudden outbreak and patchy expansion at the root collar during the middle stage, and high and uniform abundance in the advanced stage. Time-course branch inoculation experiments further showed that the pathogen first established dense populations near the inoculation site, then spread asymptomatically to distal tissues, followed by synchronized population surges across multiple stem segments during the intermediate and late stages. Microbial Communities profiling revealed that, compared with the stable structural characteristics of the endophytic bacterial community in healthy eucalyptus trees, at the intermediate stage, the xylem endophytic community transitioned from a critically reorganized state characterized by the coexistence of diverse taxa to a collapsed stable state overwhelmingly dominated by Ralstonia . Collectively, these findings indicate that eucalyptus bacterial wilt epidemics progress through distinct phases of early low-level spread, an intermediate breakthrough, and a late-stage outbreak. Pathogen-driven dysbiosis and collapse of the xylem microecosystem may therefore represent a key mechanism underlying rapid disease outbreaks, with collapse of the xylem endophytic microbial communities serving as a sentinel biomarker marking a critical transition in disease progression.