Live tracking of a plant pathogen outbreak reveals rapid and successive, multidecade episome reduction

Abstract

Quickly understanding the genomic changes that lead to pathogen emergence is necessary to launch mitigation efforts and reduce harm. Often the evolutionary events that result in an epidemic typically remain elusive long after an outbreak, which is particularly true for plant pathogens. To rapidly define the consequential evolutionary events result in pathogen emergence, we tracked in real-time a 2022 bacterial plant disease outbreak in US geranium (Pelargonium x hortorum) caused by Xhp2022, a novel lineage of Xanthomonas hortorum. Genomes from 31 Xhp2022 isolates from seven states showed limited chromosomal variation, and all contained a single plasmid (p93). Time tree and SNP whole genome analysis estimated that Xhp2022 emerged in the early 2020s. Phylogenomic analysis determined that p93 resulted from cointegration of three plasmids (p31, p45, and p66) present in a 2012 outbreak. p31, p45 and p66 were individually found in varying abundance across X. hortorum isolates from historical outbreaks dating to 1974 suggesting these plasmids were maintained in the broader metapopulation. p93 specifically arose from two co-integration events from homologous and Tn3 and XerC-mediated site-specific recombination. Although p93 suffered a 49kb nucleotide reduction, it maintained critical fitness gene functions encoding, for example, metal resistance and virulence factors, which were likely selected by the ornamental production system. Overall we demonstrate how rapid sequencing of current and historical isolates track the evolutionary history of an emerging, ongoing threat. We show a recent, tractable event of genome reduction for niche adaptation typically observed over millennia in obligate and fastidious pathogens.

Diversification of an emerging bacterial plant pathogen; insights from the global spread ofXanthomonas euvesicatoriapv.perforans

“…Whole genome analysis of X. hortorum pv. pelargonii strains from a 2022 epidemic of bacterial blight of geranium in the USA showed zero to seven chromosomal SNPs among isolates of the emergent strain that distributed to multiple states in plant cuttings 60,61 .…”