Escherichia coli O157:H7 Strain Origin, Lineage, and Shiga Toxin 2 Expression Affect Colonization of Cattle

Abstract

Enterohemorrhagic Escherichia coli O157:H7 has evolved into an important human pathogen with cattle as the main reservoir. The recent discovery of E. coli O157:H7-induced pathologies in challenged cattle has suggested that previously discounted bacterial virulence factors may contribute to the colonization of cattle. The objective of the present study was to examine the impact of lineage type, cytotoxin activity, and cytotoxin expression on the amount of E. coli O157:H7 colonization of cattle tissue and cells in vitro. Using selected bovine-and human-origin strains, we determined that lineage type predicted the amount of E. coli O157:H7 strain colonization: lineage I > intermediate lineages > lineage II. All E. coli O157:H7 strain colonization was dose dependent, with threshold colonization at 10 3 to 10 5 CFU and maximum colonization at 10 7 CFU. We also determined that an as-yet-unknown factor of strain origin was the most dominant predictor of the amount of strain colonization in vitro. The amount of E. coli O157:H7 colonization was also influenced by strain cytotoxin activity and the inclusion of cytotoxins from lineage I or intermediate lineage strains increased colonization of a lineage II strain. There was a higher level of expression of the Shiga toxin 1 gene (stx 1 ) in human-origin strains than in bovine-origin strains. In addition, lineage I strains expressed higher levels of the Shiga toxin 2 gene (stx 2 ). The present study supports a role for strain origin, lineage type, cytotoxin activity, and stx 2 expression in modulating the amount of E. coli O157:H7 colonization of cattle.Enterohemorrhagic Escherichia coli O157:H7 is a bacterium that causes serious human disease outbreaks through the consumption of contaminated food or water (39). Mature cattle are considered the primary reservoir for E. coli O157:H7 and historically were reported to have no symptoms or pathologies (17,23,38); this was attributed both to a lack of receptors for a critical E. coli O157:H7 virulence factor, Shiga toxin 1 (Stx1 [29]), and to a differential expression of type III protein secretion system effector molecules such as EspA, EspD, and Iha (25,30) in cattle compared to humans. In 2008, it was established for the first time that E. coli O157:H7 causes mild to severe intestinal pathology in persistent shedding cattle (5,26) and that the secreted cytotoxins enhanced E. coli O157:H7 colonization of intestinal tissues of cattle (6). This suggested that cattle were susceptible to E. coli O157:H7 infection and that previously discounted virulence factors could influence the amount of colonization in cattle.Three distinct E. coli O157:H7 lineages have been identified based on the lineage specific polymorphism assay (LSPA-6) that suggests both the evolutionary history of the strain and their propensity to be present among animals, the environment, and clinical human isolates (21,22,24,33,40,42). Typically, two predominant lineages have been described, lineages I and II (22,40) and, more recently, intermediate lineages that have...

Multivariate Analyses Revealed Distinctive Features Differentiating Human and Cattle Isolates of Shiga Toxin-Producing Escherichia coli O157 in Japan

“…The difference may be explained by recent reports describing the importance of genotypic and phenotypic heterogeneity of STEC O157 for virulence and adaptation to the host environment. Lowe et al (18) and Zhang et al (37) showed higher levels of adherence to intestinal cells and Shiga toxin production in LI strains than in LII strains. For stx genotypes, many researchers have found a correlation between the stx 2 gene and disease severity in humans (3,5,19).…”

Variability of Escherichia coli O157 Strain Survival in Manure-Amended Soil in Relation to Strain Origin, Virulence Profile, and Carbon Nutrition Profile

“…This corresponds to the mounting evidence that suggests there is considerable phenotypic diversity among animal-and human-associated isolates. E. coli O157 strains of animal origin showed much higher colonization of cattle tissue and cells in vitro than human-origin strains (41). The average acid resistance of bovine-biased genotypes was significantly higher than that of human strains (56,63), and bovine-biased genotypes are equipped with a more efficient nitrogen regulatory response system that enhanced survival under ammonia-limiting conditions (63).…”

Characterization of Haemorrhagic Enteritis in Dairy Goats and the Effectiveness of Probiotic and Prebiotic Applications in Alleviating Morbidity and Production Losses

“…There is one case report documenting a chronic STEC infection in a weaning kid [34] with the adherent pathogen identified as E. coli O103:H2, a non-O157 STEC that produced Stx. In the current study, we describe O157 and non-O157 STEC infections in adult goats with the non-O157 STEC requiring a 100 times lower exposure dose when compared with the O157 STEC to achieve the same colonization [33,35]. This is a remarkable virulence factor that may have contributed to the rapid onset of symptoms observed in the goats.…”