Genomic dissection of Escherichia marmotae provides insights into diversity and pathogenic potential

Anthropogenic activities enhance the interconnection of human, animal, and environmental habitats and drive the evolution and inter-niche transmission of bacteria. Clear identification of emerging bacteria and pathogen control is therefore a public health priority. In 2015, the novel Escherichia species Escherichia marmotae was assigned, but due to the lack of appropriate detection and typing technologies, the One Health impact of this species is still being unraveled. E. marmotae represents a missing link in the impact of Escherichia spp. Here, we report 25 E. marmotae identified by next-generation sequencing that were previously phenotypically characterized as Escherichia coli during national zoonosis monitoring of food-producing animals. Applying fastANI to 153 738 published Escherichia spp. genome assemblies, we identified further 124 E. marmotae, originally classified as E. coli. Phylogenomics of all 149 isolates reveals an undefined population structure that is independent of the ecological niche. We highlight the phenotypic, genomic, and plasmid diversity of E. marmotae and provide evidence for gene flow across the species. The latter is illustrated by the acquisition of antibiotic resistance plasmids and pathogenicity islands, such as the type III secretion system. Thus, our comprehensive genomic overview of an emerging potential opportunistic pathogen underlines the importance of improved detection and characterization.