Emergence and host range expansion of an epidemic lineage of Ralstonia solanacearum

An outbreak of lethal wilt disease in Martinique revealed the emergence of a new lineage (Ralstonia solanacearum IIB-4NPB) with the broadest documented host range sampled during natural infections. Another pathogen lineage (R. pseudosolanacearum I-18) expanded in parallel but retained specialisation on solanaceaous hosts. Whole-genome sequencing of 407 outbreak isolates shows both lineages disseminated from mainland populations into Martinique, where there are spatial hotspots of mobile element exchange between co-occurring lineages. The emergent lineage carries expanded CRISPR arrays and multiple prophage, along with a new family of integrative and conjugative elements (ICEs). These ICEs have two distinct cargo gene hotspots that display remarkable functional differentiation despite variable gene content, maintaining metabolism-associated functions in one and defence-related functions in the other. Our findings indicate horizontal transfer – rather than variation in canonical virulence factors – drove the emergence of IIB-4NPB by enhancing microbial metabolic capacity and anti-viral defences. This likely improved pathogen fitness in soil and host environments, increasing the likelihood of successful colonisation events.