Conditional expression of flagellar motility, curli fimbriae, and biofilms in Shiga toxin-producing Escherichia albertii

Authors: Carter, Michelle; Carychao, Diana; LINDSEY, REBECCA - Centers For Disease Control And Prevention (CDC) - United States

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/14/2024
Publication Date: 9/9/2024
Citation: Carter, M.Q., Carychao, D.K., Lindsey, R.L. 2024. Conditional expression of flagellar motility, curli fimbriae, and biofilms in Shiga toxin-producing Escherichia albertii. Frontiers in Microbiology. 15. Article 1456637. https://doi.org/10.3389/fmicb.2024.1456637.
DOI: https://doi.org/10.3389/fmicb.2024.1456637

Interpretive Summary: Biofilms of foodborne pathogens can enhance their survival and persistence in diverse ecological niches and serve as sources of contamination in food production environments and of infection in health-care environments. Adhesion is the first step in biofilm development and in establishing colonization in animal hosts. Strong adherence often implies enhanced surface attachment and biofilm formation, leading to increased fitness and pathogenic potential. In this study, we systematically examined genes encoding fimbrial and nonfimbrial adhesins in a set of E. albertii strains isolated from infected humans or from wild birds, and identified common and strain specific colonization factors. We further compared biofilm-forming ability between clinical and avian strains and identified an avian strain exhibiting high cytotoxicity and producing strong biofilms. The increased biofilm-forming ability in this avian strain was likely attributed to the acquisition of genes encoding the CFA adhesive fimbriae that are predominantly present in enterotoxigenic E. coli strains. Our study provided valuable information on molecular targets for blocking colonization of E. albertii on environmental surfaces and in animal hosts.

Technical Abstract: Escherichia albertii is an emerging foodborne pathogen. We previously reported that some avian Shiga toxin-producing E. albertii strains exhibited higher or comparable cytotoxicity with several enterohemorrhagic E. coli (EHEC) outbreak strains. To better understand the environmental persistence of this pathogen, comparative genomics and phenotypic assays were carried out to assess adhesion capability, motility, and biofilm formation in E. albertii. Among the 108 genes involved in biogenesis of fimbrial and nonfimbrial adhesins, genes related to curli fimbriae, hemorrhagic E. coli pilus, type 1 fimbriae, and Sfm fimbriae were conserved in E. albertii. All 20 E. albertii strains carried a complete set of primary flagellar genes that were organized into four genes clusters, while five strains possessed genes involved in biogenesis of the secondary flagella, also known as lateral flagella. Compared to EHEC strain EDL933, the eight chemotaxis genes located within the primary flagellar genes clusters were deleted in all E. albertii strains. Additional deletions of motility genes flhABCD and motBC were identified in several E. albertii strains. Swimming motility was detected in three E. albertii strains when grown in LB medium, however, when grown in 5% TSB or in the pond water-supplemented with 10% pigeon dropping, four non-motile strains became motile. Although all E. albertii strains carried curli genes, curli fimbriae were detected in four, five, and eight strains following 24, 48, and 120 h incubation, respectively. Strong biofilms were detected in strains that produced curli fimbriae and in a chicken isolate that was curli fimbriae negative but carried genes encoding adhesive fimbriae K88, a signature of enterotoxigenic E. coli strains causing neonatal diarrhea in piglets. For any of the phenotypic traits examined, no correlation was revealed between the strains isolated from different sources, or between the strains with and without Shiga toxin genes. The phenotypic variations could not be explained by the genetic diversity or the difference in adhesin genes repertoire, implying complex regulation in expression of various adhesins. An avian strain isolated from an American crow exhibited a high level of cytotoxicity and was also a strong biofilm producer, implying its potential in emerging into a high-risk pathogen.