Inferring the Evolutionary History of the Plant Pathogen Pseudomonas syringae from Its Biogeography in Headwaters of Rivers in North America, Europe, and New Zealand

ABSTRACT Nonhost environmental reservoirs of pathogens play key roles in their evolutionary ecology and in particular in the evolution of pathogenicity. In light of recent reports of the plant pathogen Pseudomonas syringae in pristine waters outside agricultural regions and its dissemination via the water cycle, we have examined the genetic and phenotypic diversity, population structure, and biogeography of P. syringae from headwaters of rivers on three continents and their phylogenetic relationship to strains from crops. A collection of 236 strains from 11 sites in the United States, in France, and in New Zealand was characterized for genetic diversity based on housekeeping gene sequences and for phenotypic diversity based on measures of pathogenicity and ice nucleation activity. Phylogenetic analyses revealed several new genetic clades from water. The genetic structure of P. syringae populations was not influenced by geographic location or water chemistry, whereas the phenotypic structure was affected by these parameters. Comparison with strains from crops revealed that the metapopulation of P. syringae is structured into three genetic ecotypes: a crop-specific type, a water-specific type, and an abundant ecotype found in both habitats. Aggressiveness of strains was significantly and positively correlated with ice nucleation activity. Furthermore, the ubiquitous genotypes were the most aggressive, on average. The abundance and diversity in water relative to crops suggest that adaptation to the freshwater habitat has played a nonnegligible role in the evolutionary history of P. syringae. We discuss how adaptation to the water cycle is linked to the epidemiological success of this plant pathogen. IMPORTANCE Many pathogens have life cycles that involve survival and multiplication in nonhost environmental habitats. For human pathogens, numerous studies have revealed how adaptation to environmental habitats is linked to the evolution of their pathogenicity and emergence of pathogens. For plant pathogens, the link between adaptation to nonhost habitats and pathogenicity has not been explored. Here we have examined the genetic and phenotypic diversity of the plant pathogen Pseudomonas syringae in headwaters of rivers on three continents and compared it to that of strains from crops. This model pathogen was chosen because it is widely abundant in habitats associated with the water cycle and in particular in pristine waters outside agricultural regions. This work reveals that there is considerable exchange of populations between freshwater and agricultural habitats and that those in the former contribute considerably to the diversification of P. syringae. Many pathogens have life cycles that involve survival and multiplication in nonhost environmental habitats. For human pathogens, numerous studies have revealed how adaptation to environmental habitats is linked to the evolution of their pathogenicity and emergence of pathogens. For plant pathogens, the link between adaptation to nonhost habitats and pathogenicity has not been explored. Here we have examined the genetic and phenotypic diversity of the plant pathogen Pseudomonas syringae in headwaters of rivers on three continents and compared it to that of strains from crops. This model pathogen was chosen because it is widely abundant in habitats associated with the water cycle and in particular in pristine waters outside agricultural regions. This work reveals that there is considerable exchange of populations between freshwater and agricultural habitats and that those in the former contribute considerably to the diversification of P. syringae.