Interaction Between Climatic Variation and Pathogen Diversity Shape Endemic Disease Dynamics in the Agricultural...

Endemic pathogens continue to pose threats of recurring outbreaks, especially in agricultural settings. How these outbreaks unfold and what drives the variability in disease epidemics is less understood. We addressed this question in the Xanthomonas-tomato pathosystem by developing an integrated approach that linked the within-field quantitative signature of local pathogen diversity to climatic conditions to explain variable bacterial disease epidemics across fields. Using strain-resolved metagenomics, we found that pathogen heterogeneity with multiple co-occurring lineages is common. Higher disease severity was associated with higher pathogen diversity. Considering these observations, we used response-specific regression models to investigate the role of environmental variables in driving differences in disease and strain dynamics. Abrupt and frequent changes in environmental factors explained the variability of disease severity. We observed variable lineage dynamics across fields, but at least two lineages with divergent, climate-dependent fitness strategies coexisted throughout the growing season without either of them taking the lead. We further profiled the dynamics of single-nucleotide polymorphism variants in the pathogen population and observed that some alleles are temporarily favoured by specific climatic conditions encountered throughout the growing season, leading to oscillating seasonal patterns of allelic frequencies. These alleles can be referred to as seasonal alleles. Overall, our study revealed that the seasonal fluctuations in pathogen strain composition, diversity and climate-influenced pathogen fitness play a significant role in shaping the severity and variability of bacterial spot disease outbreaks.