A clonal shiga toxin-producing Escherichia coli O121:H19 population exhibits diverse carbon utilization patterns

Authors: Carter, Michelle; TAN, ZHONGFANG - HENAN UNIVERSITY; PHAM, ANTARES; Carychao, Diana; COOLEY, MICHAEL

Submitted to: Foodborne Pathogens and Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/3/2019
Publication Date: 3/8/2019
Citation: Carter, M.Q., Tan, Z., Pham, A.C., Carychao, D.K., Cooley, M.B. 2019. A clonal shiga toxin-producing Escherichia coli O121:H19 population exhibits diverse carbon utilization patterns. Foodborne Pathogens and Disease. 16(6):384-393. https://doi.org/10.1089/fpd.2018.2567.
DOI: https://doi.org/10.1089/fpd.2018.2567

Interpretive Summary: Shiga toxin-producing Escherichia coli (STEC) is historically classified based on O and H antigens. Serotype O121 is one of the seven major serotypes associated with severe human disease. Numerous SETC O121 strains were isolated from Salina, California, a major produce production region in the US. In this study, we investigated the potential of the environmental STEC O121 strains to cause disease in humans and to persist in natural environments. We found that majority of environmental STEC O121 strains contain genes encoding key virulence traits of enterohemorrhagic E. coli, a sub-group of STEC capable of causing hemolytic uremic syndrome in humans. Among the STEC O121:H19 strains that are genotypically indistinguishable, large variation in carbon utilization pattern was observed, including the enhanced metabolic potential for plant- or mucus-derived substrates in several isolates. Our study suggests that niche (environment) selection is an important factor in evolution of STEC. Strains or variants with improved ability to grow on diverse carbon substrates that are accessible in soil, on plants, or in gastrointestinal tract would have been selected and serve as a source of hyper-virulent STEC strains.

Technical Abstract: Shiga toxin-producing Escherichia coli (STEC) serotype O121 is one of the major non-O157 serotypes associated with severe human disease. Here we examined the population structure, virulence potential, and metabolic pro'le of environmental STEC O121 strains recovered from a major produce production region in California, and performed comparative analyses with STEC O121 clinical isolates. Multi locus sequence typing (MLST) revealed that sequence type (ST)-655, a common ST in clinical strains, was the predominant genotype among the environmental strains. Phylo-typing placed all STEC O121 strains in the B1 group, a lineage containing other major non-O157 sero-groups of STEC. Genes encoding different subtypes of Shiga toxin 1 and 2 were detected in O121 including stx1a, stx1d, stx2a, and stx2e. Furthermore, genes encoding intimin (eae) and enterohemolysin (ehxA) were detected in a majority of environmental strains (83.3%), revealing that the majority of environmental STEC O121 strains are enterohemorrhagic E. coli (EHEC). Clustering analysis based on the carbon utilization pattern placed the O121 strains with the same genotype together. Among the 122 carbon substrates that supported the growth of all or some STEC O121 strains, 44 and 35 exhibited ST and strain specific metabolic profiles, respectively. Variations in curli biogenesis and swimming motility were also detected in ST-655 strains, suggesting the existence of diverse phenotypic variants in STEC clonal populations. Environmental ST-655 strains were indistinguishable from clinical strains either by MLST typing or carbon utilization profiling, indicating a conservation of virulence and fitness traits in environmental strains. Considering the ecological niches that STEC colonizes, improved metabolic potential for plant-derived carbohydrates, mucus-derived substrates, or secondary metabolites produced by the indigenous microorganisms would confer STEC competitive traits that facilitate survival and adaptation of STEC population to a given niche including infected humans.