Population genomic analysis of an emerging pathogen Lonsdalea quercina affecting various species of oaks in western North America

Previously unrecognized diseases continue to threaten the health of forest ecosystems globally. Understanding processes leading to disease emergence is important for effective disease management and prevention of future epidemics. Utilizing whole genome sequencing, we studied the phylogenetic relationship and within diversity of two populations of the bacterial oak pathogen Lonsdalea quercina from western North America (Colorado and California) and compared these populations to other Lonsdalea species found worldwide. Phylogenetic analysis separated Colorado and California populations into two well supported clades within the genus Lonsdalea, with an average nucleotide identity between them near species boundaries (95.31%) for bacteria, suggesting long isolation. Populations comprise distinct patterns in genetic structure and distribution. Genotypes collected from different host species and habitats were randomly distributed within the California cluster, while most Colorado isolates from introduced planted trees were distinct from isolates collected from a natural stand of CO native Q. gambelii, indicating the presence of cryptic population structure. The distribution of clones in California varied, while Colorado clones were always collected from neighboring trees. Despite its recent emergence, the Colorado population had higher nucleotide diversity, possibly due to migrants moving with nursery stock. Overall results suggest independent pathogen emergence in two states likely driven by changes in host-microbe interactions due to ecosystems conditions changes. To our knowledge, this is the first study on L. quercina population structure. Further studies are warranted to understand evolutionary relationships among L. quercina populations from different areas, including the native habitat of red oak in northeastern USA. ImportanceBacterial pathogens from genus Lonsdalea severely affect oak forest ecosystems worldwide. In Colorado, USA, L. quercina is one of the causal agents of drippy blight disease on introduced red oak trees. Prior to discovery of drippy blight in Colorado, L. quercina was reported on oak trees in California, causing drippy nut on acorns of native oaks. Due to its recent emergence in Colorado, the origin and movement of L. quercina are unknown. In this study we investigated evolutionary relationships within genus Lonsdalea worldwide and L. quercina population structure in western USA. Our results demonstrate that L. quercina Colorado and California populations comprise distinct patterns of genetic structure and distribution, suggesting that accidental pathogen introduction from California to Colorado is unlikely. Higher nucleotide diversity in a recently emerged Colorado population suggests the bacterial strains might be migrants that initially moved with nursery stock from other areas in the last century. For example, Colorado strains of L. quercina may have moved from native stands of red oaks in the northeastern or southern USA. Curiously, however, this disease is not known in native red oak in the northeastern USA. Initial causes of recent disease emergence are likely driven by environmental/ecosystem changes since isolates for this study were collected from established mature trees. Results presented here give a better understanding of population biology of the bacterial oak pathogen and provide a framework for investigation of evolutionary relationships among pathogen populations from different areas.