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 ecosystem conditions changing.
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.

此前未被识别的病害持续威胁着全球森林生态系统的健康。理解病害出现的过程对于有效管理病害和预防未来疫情至关重要。利用全基因组测序（whole genome sequencing）技术，我们研究了北美西部（科罗拉多州和加利福尼亚州）两种橡树细菌性病原菌Lonsdalea quercina种群的系统发育关系及其内部多样性，并将这些种群与全球范围内发现的其他Lonsdalea物种进行了比较。系统发育分析（phylogenetic analysis）将科罗拉多州和加利福尼亚州的种群划分为Lonsdalea属内两个支持度较高的分支（clade），两者之间的平均核苷酸一致性（average nucleotide identity）接近细菌的物种边界（95.31%），表明它们长期处于隔离状态。这些种群在遗传结构和分布上呈现出明显不同的模式。从加利福尼亚集群中不同宿主物种和栖息地收集的基因型呈随机分布；而科罗拉多州从引种栽培树木中分离出的大多数菌株与从CO本地Q. gambelii天然林分中分离出的菌株明显不同，这表明存在隐秘的种群结构。加利福尼亚州的克隆分布多样，而科罗拉多州的克隆则总是从相邻树木中收集到。尽管科罗拉多种群是近期出现的，但其核苷酸多样性更高，这可能是由于病原菌随苗木迁移所致。总体结果表明，这两个州的病原菌独立出现，可能是由于生态系统条件变化导致宿主-微生物相互作用改变所驱动。据我们所知，这是首次针对L. quercina种群结构开展的研究。未来需进一步研究以明确不同地区（包括美国东北部红栎原生栖息地）L. quercina种群之间的进化关系。