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Background <p>Soil-borne pathogens threaten global agriculture, yet soil microbiome adaptation to persistent pathogen pressure is poorly understood. This study characterized the ecological and genomic long-term shifts in a tobacco field soil microbiome under sustained <i>Phytophthora nicotianae</i> pressure. We conducted a six-year longitudinal metagenomic study in a field with a documented history of tobacco black shank disease. Comparative analysis of the rhizosphere microbiome from Year_1 and Year_6 was performed using shotgun sequencing, non-redundant gene catalog construction, and functional annotation against specialized databases.</p> Results <p>Our analysis revealed a profound genetic remodelling, with 45.6% (116,529) of 255,258 genes showing significant differences in abundance (<i>p</i> &lt; 0.05, |<i>log</i><sub><i>2</i></sub>FC| ≥ 1). This restructuring was systematic, characterized by significant enrichment of the soil antibiotic resistome, where 45.88% of antibiotic resistance genes were differentially abundant and showed a distinct trend toward increased abundance. The functional potential for carbohydrate metabolism was reorganized, with 53.2% of CAZymes (Carbohydrate-Active enZYmes) genes showing differential abundance and a predominant depletion. Analysis of COG (Clusters of Orthologous Groups) revealed a strategic functional trade-off, with significant enrichment of defense-related categories like secondary metabolite biosynthesis (+ 52.9%) alongside a reduction in growth-related processes. Such functional changes were ultimately driven by an taxonomically homogenized community, as indicated by a major reduction in species level alpha diversity (Shannon index: 5.52 to 5.31) that coexisted with a 14.8% significant increase in species level abundance, which showed a selective enrichment of a subset of dominant taxa.</p> Conclusion <p>Sustained pathogen pressure triggers a coordinated, multi-level adaptive succession, reshaping the genetic, functional, and taxonomic structure of the soil microbiome into a more defended and specialized state.</p>

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Ecological and genomic dynamics of the soil microbiome under sustained pressure from Phytophthora nicotianae, the causal agent of tobacco black shank disease

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2026年5月14日

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  • Umer Basu,
  • Shafat Ahmad Ahanger,
  • Tianyu Song,
  • Xiaotong Gai,
  • Xiaoping Hu

摘要

Background

Soil-borne pathogens threaten global agriculture, yet soil microbiome adaptation to persistent pathogen pressure is poorly understood. This study characterized the ecological and genomic long-term shifts in a tobacco field soil microbiome under sustained Phytophthora nicotianae pressure. We conducted a six-year longitudinal metagenomic study in a field with a documented history of tobacco black shank disease. Comparative analysis of the rhizosphere microbiome from Year_1 and Year_6 was performed using shotgun sequencing, non-redundant gene catalog construction, and functional annotation against specialized databases.

Results

Our analysis revealed a profound genetic remodelling, with 45.6% (116,529) of 255,258 genes showing significant differences in abundance (p < 0.05, |log2FC| ≥ 1). This restructuring was systematic, characterized by significant enrichment of the soil antibiotic resistome, where 45.88% of antibiotic resistance genes were differentially abundant and showed a distinct trend toward increased abundance. The functional potential for carbohydrate metabolism was reorganized, with 53.2% of CAZymes (Carbohydrate-Active enZYmes) genes showing differential abundance and a predominant depletion. Analysis of COG (Clusters of Orthologous Groups) revealed a strategic functional trade-off, with significant enrichment of defense-related categories like secondary metabolite biosynthesis (+ 52.9%) alongside a reduction in growth-related processes. Such functional changes were ultimately driven by an taxonomically homogenized community, as indicated by a major reduction in species level alpha diversity (Shannon index: 5.52 to 5.31) that coexisted with a 14.8% significant increase in species level abundance, which showed a selective enrichment of a subset of dominant taxa.

Conclusion

Sustained pathogen pressure triggers a coordinated, multi-level adaptive succession, reshaping the genetic, functional, and taxonomic structure of the soil microbiome into a more defended and specialized state.