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Tobacco black shank, caused by Phytophthora nicotianae, is a devastating soil-borne disease. However, the microecological factors controlling its occurrence remain unclear. In this study, we first correlated disease severity with soil properties across 72 fields, identifying Soil organic carbon (SOC) as the key environmental factor after pathogen abundance. To elucidate its role, we integrated SOC component analysis, metagenomic sequencing, and microbial cultivation to associate SOC composition with shifts in microbiome structure and function. The results showed that as disease severity increased, the α-diversity of the rhizosphere microbial community decreased and its structure simplified. This was accompanied by a significant reduction in antagonistic taxa such as Streptomyces and a shift in dominant phyla from Actinomycetota to Nitrososphaerota. Functional analysis revealed that disease progression significantly altered the carbohydrate metabolic potential of the rhizosphere microbiome, manifested as an increased potential for lignin degradation and a significantly decreased potential for microbial necromass carbon (MNC) degradation. Analysis SOC components revealed that the contents of ferulic acid, vanillic acid, and particulate organic carbon (POC) decreased with disease severity, showing negative correlations with pathogen abundance. In contrast, MNC content increased with disease severity and exhibited a strong positive correlation with pathogen abundance. Structural equation modeling (SEM) analysis revealed the complex pathways through which different organic carbon components influence disease severity. The findings not only deepen the theoretical understanding of the "carbon–microbe–disease" interplay in rhizosphere microecology, but also provide key targets and strategic foundations for achieving green, ecological control of tobacco black shank through soil carbon management.
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