Abstract
Copper-based antimicrobial compounds are widely used to control plant bacterial pathogens. Pathogens have adapted in response to this selective pressure. Xanthomonas citri pv. citri, a major citrus pathogen causing Asiatic citrus canker, was first reported to carry plasmid-encoded copper resistance in Argentina. This phenotype was conferred by the copLAB gene system. The emergence of resistant strains has since been reported in Réunion and Martinique. Using microsatellite-based genotyping and copLAB PCR, we demonstrated that the genetic structure of the copper-resistant strains from these three regions was made up of two distant clusters and varied for the detection of copLAB amplicons. In order to investigate this pattern more closely, we sequenced six copper-resistant X.citri pv.citri strains from Argentina, Martinique and Réunion, together with reference copper-resistant Xanthomonas and Stenotrophomonas strains using long-read sequencing technology. Genes involved in copper resistance were found to be strain dependent with the novel identification in X.citri pv.citri of copABCD and a cus heavy metal efflux resistance-nodulation-division system. The genes providing the adaptive trait were part of a mobile genetic element similar to Tn3-like transposons and included in a conjugative plasmid. This indicates the system's great versatility. The mining of all available bacterial genomes suggested that, within the bacterial community, the spread of copper resistance associated with mobile elements and their plasmid environments was primarily restricted to the Xanthomonadaceae family.
Highlights
The dynamics of genome evolution differ considerably across the bacterial diversity spectrum
By combining population genetics based on microsatellite and minisatellite markers, comparative genomics and network analysis, we address the following questions: how do copper-resistant strains from the three outbreaks relate to each other? Are the genes responsible for copper resistance similar for the different outbreaks of X. citri pv. citri? What is the genomic environment of these genes and how does it vary within pathovar citri and among xanthomonads? We discuss the evolutionary implications of our findings and propose future lines of research to increase our understanding of how adaptive genes spread in bacterial communities
We provide a comparative genomic analysis of plasmids associated with CuR in several Xanthomonas species, including X. citri pv. citri
Summary
The dynamics of genome evolution differ considerably across the bacterial diversity spectrum. The presence of assisted or autonomous mobility genetic elements determines the plasmids’ ability to be mobilizable or conjugative (Smillie et al 2010) Due to their relative stability in the plasmid genome, backbone genes may show traces of adaptation to bacterial hosts (Norberg et al 2011). Accessory genes are often located on mobile genetic elements themselves, either transposons (Haines et al 2007; Trefault et al 2004) or integrons (Tennstedt et al 2005), defining hot spots of insertions within the plasmid genome These elements are generally autonomous and can be transferred between genera, families and even kingdoms (Heinemann & Sprague 1989). It is obvious that in genetically monomorphic pathogens as in others, in order to further our understanding of bacterial adaptation and ecology, we need to understand plasmid evolutionary dynamics, i.e. deciphering the genomic structure of plasmids and the mechanisms involved in plasmid spread among bacteria. While several studies have already documented the history of specific accessory genes (Perry & Wright 2013), very few studies have documented the evolution of the whole plasmid genome for a given ecological function (but see Norberg et al (2011) for a study of the backbone genome of IncP-1 plasmid family)
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