Four Decades of Genomic Stability and Adaptive Divergence in Xanthomonas arboricola pv. pruni-Infecting Phages: Defining Duraznoxanthovirus arenicola and Its Evolutionary Framework

Abstract

Bacteriophages (phages) are abundant and ecologically significant, yet their diversity and roles in plant-associated ecosystems remain poorly understood, limiting their application in sustainable disease management. To address this gap, we characterized 15 phages infecting Xanthomonas arboricola pv. pruni, the causal agent of bacterial spot on peach, has been isolated for over four decades from North Carolina orchards. Comparative genomic and phylogenetic analyses revealed two temporally distinct clades with >95% nucleotide identity and 63 conserved core genes, forming a new genus and species, Duraznoxanthovirus arenicola. These findings challenge assumptions of pervasive genomic mosaicism, highlighting remarkable genomic stability alongside localized variability in accessory loci. Beyond genus-level characterization, our analyses support a broader taxonomic restructuring within the family Anamaviridae, introducing a new subfamily (Terravirinae) and two new genera (Duraznoxanthovirus and Ralstopathovirus). This work provides the first family-level framework for phages exclusively infecting plant-associated bacteria, offering evolutionary insights and a foundation for ecological studies and management strategies.