Pathogenicity assessment of Shiga toxin-producing Escherichia coli strains isolated from wild birds in a major agricultural region in California

Authors: Carter, Michelle; Quinones, Beatriz; Laniohan, Nicole; Carychao, Diana; Pham, Antares; He, Xiaohua; COOLEY, MICHAEL - Retired ARS Employee

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/11/2023
Publication Date: 9/26/2023
Citation: Carter, M.Q., Quinones, B., Laniohan, N.S., Carychao, D.K., Pham, A.C., He, X., Cooley, M. 2023. Pathogenicity assessment of Shiga toxin-producing Escherichia coli strains isolated from wild birds in a major agricultural region in California. Frontiers in Microbiology. 14. Article 1214081. https://doi.org/10.3389/fmicb.2023.1214081.
DOI: https://doi.org/10.3389/fmicb.2023.1214081

Interpretive Summary: Current knowledge about the pathogenesis of Shiga toxin-producing Escherichia coli (STEC) is largely limited to strains of several predominant groups such as STEC O157:H7. In recent years non-O157:H7 STEC serotypes associated foodborne outbreaks and human infections have increased, thus information about virulence and pathogenesis of diverse STEC strains is desired for the development of a One Health mitigation strategy. Wildlife has been recognized as a primary source of emerging infectious diseases. Different wildlife species could harbor lesser-known or characterized STEC serotypes. In this study we systematically characterized pathogenicity potential of the three STEC strains isolated from wild birds in a major agriculture region in California and revealed novel virulence determinants in the avian STEC strains. Our study demonstrated that pathogenesis of STEC is a complex process and diverse mechanisms contribute to pathogenicity of STEC. Such information is important for risk assessment in preharvest environments and contribute to the development of effective control strategies to ensure the safety of food from farm to fork.

Technical Abstract: Shiga toxin-producing Escherichia coli (STEC) consists of diverse strains differing in genetic make-up and virulence potential. To better understand the pathogenicity potential of STEC carried by the wildlife, three STEC and one E. coli strains isolated from wild birds near a major agricultural region in California were selected for comparative pathogenomic analyses. Three American crow (Corvus brachyrhynchos) strains, RM9088, RM9513, and RM10410, belonging to phylogroup A with serotypes O109:H48, O9:H30, and O113:H4, respectively, and a red-winged blackbird (Agelaius phoeniceus) strain RM14516 in phylogroup D with serotype O17:H18, were examined. Shiga toxin genes were identified in RM9088 (stx1a), RM10410 (stx1a + stx2d), and RM14516 (stx2a). Unlike STEC O157:H7 strain EDL933, none of the avian STEC strains harbored the pathogenicity islands OI-122, OI-57, and the locus of enterocyte effacement, therefore the type III secretion system biogenesis genes and related effector genes were absent in the three avian STEC genomes. Interestingly, all avian STEC strains exhibited greater (RM9088 and RM14516) or comparable (RM10410) cytotoxicity levels compared with EDL933. Comparative pathogenomic analyses revealed that RM9088 harbored numerous genes encoding toxins, toxins delivery systems, and adherence factors, including heat-labile enterotoxin, serine protease autotransporter toxin Pic, type VI secretion systems, protein adhesin Paa, fimbrial adhesin K88, and colonization factor antigen I. RM9088 also harbored a 36-Kb high pathogenicity island, which is related to iron acquisition and pathogenicity in Yersinia spp. Strain RM14516 carried an acid fitness island like the one in EDL933, containing a nine gene cluster involved in iron acquisition. Genes encoding extracellular serine protease EspP, subtilase cytotoxin, F1C fimbriae, and inverse autotransporter adhesin IatC were only detected in RM14516, and genes encoding serine protease autotransporter EspI and P fimbriae were only identified in RM10410. Although all curli genes were present in avian STEC strains, production of curli fimbriae was only detected for RM9088 and RM14516. Consistently, strong, moderate, and little biofilms were observed for RM9088, RM14516, and RM10410, respectively. Our study revealed novel combinations of virulence factors in two avian strains, which exhibited high level of cytotoxicity and strong biofilm formation. Comparative pathogenomics is powerful in assessing pathogenicity and health risk of STEC strains.