Rapid population flux in bacterial spot xanthomonads during a transition in dominance between two genotypes in consecutive tomato production seasons and identification of a new species Xanthomonas oklahomensis sp. nov.

In the bacterial spot of tomato disease complex, Xanthomonas euvesicatoria pv. perforans (Xep) is known to outcompete X. euvesicatoria pv. euvesicatoria (Xee). The result, over time in tomato production systems where both pathogens are present, is the anticipated displacement of Xee by Xep. In this study, we characterized the population of recovered strains from grower fields in response to a bacterial spot of tomato outbreak in east and central Oklahoma in 2018 and 2019. Tomato and pepper strains sampled in earlier years were included to provide additional context. Phenotypic and genome-based analyses showed marked differences in race and species composition in recovered strains. All pre-2018 (2001-2014) tomato bacterial spot strains were Xep race T3, except one T4 strain. Tomato bacterial spot strains in 2018 consisted of Xee race T1 and Xep T3, while strains recovered in 2019 from the same locations were exclusively Xep T4 strains. The 2019 Xep T4 strains form the same cluster with the 2014 Xep T4 strain on the phylogenetic tree, suggesting the same population. Only the Xep race T4 strains showed an expanded host range to pepper. The recovered strains were also variable in copper sensitivity and effector content. We additionally recovered non-bacterial spot xanthomonads, one of which belongs to the new species, Xanthomonas oklahomensis sp. nov. These results contributes to novel insights in understanding genomic heterogeneity and seasonal population flux between competing bacterial genotypes during disease outbreaks and can be considered when developing disease management strategies.