Genomic and phenotypic characterization of Shiga toxin-producing Escherichia albertii strains isolated from wild birds in a major agricultural region in California

Authors: Carter, Michelle; Quinones, Beatriz; He, Xiaohua; Pham, Antares; Carychao, Diana; COOLEY, MICHAEL - Retired ARS Employee; LO, CHIEN-CHI - Los Alamos National Research Laboratory; CHAIN, PATRICK - Los Alamos National Research Laboratory; LINDSEY, REBECCA - Centers For Disease Control And Prevention (CDC) - United States; Bono, James - Jim

Submitted to: Microorganisms
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/16/2023
Publication Date: 11/18/2023
Citation: Carter, M.Q., Quinones, B., He, X., Pham, A.C., Carychao, D.K., Cooley, M., Lo, C., Chain, P.S., Lindsey, R.L., Bono, J.L. 2023. Genomic and phenotypic characterization of Shiga toxin-producing Escherichia albertii strains isolated from wild birds in a major agricultural region in California. Microorganisms. 11. Article 2803. https://doi.org/10.3390/microorganisms11112803.
DOI: https://doi.org/10.3390/microorganisms11112803

Interpretive Summary: Escherichia albertii, an emerging human enteropathogen and an avian pathogen, was first isolated from Bangladeshi children with diarrhea in 1991 and classified initially as Hafnia alveri. In 2003, these isolates were reclassified as E. albertii based on the improved molecular methods. Sporadic outbreaks of E. albertii infections have been reported worldwide although pathogenesis and environmental reservoirs of this foodborne pathogen are not well understood. With rapid development of Next Generation DNA Sequencing technology, genomic characterization is needed for improved detection and to understand the pathogenesis of this pathogen. In this study, ten E. albertii strains, isolated from wild birds in central California, were chosen for whole genome sequencing. The complete genome sequences were compared with the clinical strains collected by the CDC from 1954-2014 to reveal the virulence genes repertoire of E. albertii wild bird strains. Production of Shiga toxin and cytotoxicity of each strain were further examined and compared to the various Shiga toxin-producing Escherichia coli (STEC) strains, an important and common foodborne pathogen. Our study revealed novel virulence genes in E. albertii strains and identified two avain Shiga toxin-producing E. albertii (STEA) strains exhibiting significantly higher cytotoxicity than several STEC outbreak strains. Such information is valuable to elucidate the pathogenesis and disease ecology of E. albertii as well as for risk assessment in the preharvest environment.

Technical Abstract: Escherichia albertii is an emerging foodborne pathogen. To better understand the pathogenesis and health risk of this pathogen, comparative genomics and phenotypic characterization were applied to assess the pathogenicity potential of E. albertii strains isolated from wild birds in a major agricultural region in California. Shiga toxin genes stx2f were present in all avian strains. Pangenome analyses of 20 complete genomes revealed a total of 11,249 genes, of which nearly 80% were accessory genes. Both core gene-based phylogenetic and accessory gene-based relatedness analyses consistently grouped the three stx2f-positive clinical strains with the five avian strains carrying ST7971. Among the three Stx2f-converting prophage integration sites identified, ssrA was the most common one. Besides the locus of enterocyte effacement and type three secretion system, the high pathogenicity island, OI-122, and type six secretion systems were identified. Substantial strain variation in virulence gene repertoire, Shiga toxin production, and cytotoxicity were revealed. Six avian strains exhibited significantly higher cytotoxicity than that of stx2f-positive E. coli, and three of them exhibited a comparable level of cytotoxicity with that of enterohemorrhagic E. coli outbreak strains, suggesting that wild birds could serve as a reservoir of E. albertii strains with great potential to cause severe diseases in humans.