Ecology, genomics and biocontrol potential of bacteriophages infecting the bacterial wilt pathogen Ralstonia solanacearum species complex in Reunion Island

The Ralstonia solanacearum species complex (RSSC), the causal agent of bacterial wilt, is among the most destructive soil-borne plant pathogens worldwide, yet effective and sustainable control strategies remain limited. Bacteriophages represent promising biocontrol agents, but their efficacy depends on ecological compatibility with local pathogen populations. Here, we combined ecological sampling, comparative genomics, phenotypic characterization and plant assays to investigate RSSC-infecting phages in Reunion Island and evaluate their biocontrol potential. We isolated 45 phages from diverse agricultural matrices and obtained complete genome sequences for 35 novel isolates. Phylogenomic analyses revealed a locally diversified assemblage comprising multiple known taxa and several putative new genera, forming clusters largely distinct from global reference phages. Phage diversity and antibacterial activity were structured primarily by bacterial phylogeny rather than plant host or geographic origin, indicating that plants act mainly as ecological interfaces while environmental bacterial populations shape phage specialization. The community displayed two contrasting evolutionary strategies: expanding virulent lineages associated with strong antibacterial activity and persistent temperate lineages carrying integration and host-interaction functions. Host-range assays confirmed phylotype-dependent susceptibility, and strictly lytic phages showed consistently higher inhibitory activity. Guided by combined genomic and phenotypic screening, we designed a multi-family phage cocktail targeting dominant local RSSC lineages. The cocktail exhibited strong in vitro suppression of bacterial growth and significantly reduced disease severity in tomato plants. Together, our results demonstrate that effective phage biocontrol depends on evolutionary matching between phages and regional pathogen populations. Integrating ecological, genomic and functional characterization provides a robust framework for selecting locally adapted phages and developing durable phage-based strategies for managing bacterial wilt.