Time-calibrated genomic evolution of a monomorphic bacterium during its establishment as an endemic crop pathogen

The reconstruction of the evolutionary histories of pathogen populations in space and time often improves our understanding of their epidemiology. However, analyses are usually restricted to the nonrecombining genomic regions and, thus, fail to inform on the dynamics of the accessory genome. Yet, horizontal gene transfer is of striking importance to the evolution of bacteria as it can redistribute phenotypically important genes.

For bacterial pathogens, those include resistance to antimicrobial compounds and virulence factors. Although understanding the gene turnover in genomes at microevolutionary scales is key to apprehend the pace of this evolutionary process, few studies are available. Here we addressed this question for the epidemic lineage of Xanthomonas citri pv. citri, a bacterial plant pathogen of major agricultural importance worldwide. Relying on a dense geographic sampling spanning 39 years of evolution, we estimated both the dynamics of Single Nucleotide Polymorphism accumulation and the gene content turnover.

We showed extensive gene content variation among the lineage even at the smallest phylogenetic and geographic scales. Gene turnover rate exceeded SNP mutation rates by three orders of magnitude. Accessory genes were preferentially plasmid-encoded, but we evidenced a highly plastic chromosomal region hosting ecologically important genes such as transcription activator-like effectors. We argue that turnover of accessory genes provides a potent evolutionary force in monomorphic bacteria, and exemplify this statement retracing the history of a mobile element conferring resistance to copper compounds widely used for the management of plant bacterial pathogens.