Abstract
The host mechanisms involved in Escherichia coli O157 super-shedding in cattle is largely unknown. In this study, the comparison of transcriptomes of intestinal tissues between super-shedders (SS) and cattle negative for E. coli O157 (NS) was performed, aiming to identify genes that are potentially associated with super-shedding. In total, 16,846 ± 639 (cecum) to 18,137 ± 696 (distal jejunum) were expressed throughout the intestine, with the expressed genes associated with immune functions more pronounced in the small intestine. In total, 351 differentially expressed (DE) genes were identified throughout the intestine between SS and NS, with 101 being up-regulated and 250 down-regulated in SS. Functional analysis revealed DE genes were involved in increased T-cell responses and cholesterol absorption in the distal jejunum and descending colon, and decreased B-cell maturation in the distal jejunum of SS. RNA-Seq based SNP discovery revealed that the mutations in seven DE genes involved in leukocyte activation and cholesterol transportation were associated with E. coli O157 shedding. Our findings suggest that T-cell responses and cholesterol metabolism in the intestinal tract may be associated with super-shedding phenomenon, and the SNPs in the DE genes are possibly associated with the observed gene expression difference between SS and NS.
Highlights
The sustainable agriculture production concept of “from farm gate to food plate” makes food safety an important component through the beef production chain
Principal component analysis (PCA) plots based on the whole transcriptome revealed that four of the NS were clustered closely for duodenum, cecum and spiral colon, three of NS were clustered closely for distal jejunum, and NS and SS were separated on the direction of first principal component for descending colon (Fig. 2)
Our results suggest that (1) the bovine small intestine may have a more active immune system than the large intestine, making the distal colon towards rectum more prone to colonisation with E. coli O157; (2) the distal jejunum and descending colon of SS showed potentially higher levels of T-cell migration and proliferation, and cholesterol absorption, as well as inhibited B-cell maturation (Fig. 6A); (3) host genetic variation may be one of the mechanisms to affect the expression of genes involved in immune function and cholesterol absorption that may play a role in E. coli O157 shedding in SS, but genetic association analysis with larger number of animals is required to validate such speculation
Summary
The sustainable agriculture production concept of “from farm gate to food plate” makes food safety an important component through the beef production chain. Host, and microbes have been proposed to affect super-shedding[5]. With regard to the microbial factors, in vitro studies have revealed that several E. coli O157 non-LEE (locus for enterocyte effacement)-encoded type III effector proteins may impair host innate immunity and that Shiga toxins can repress lymphocytes responses[7, 8], which could lead to potential colonisation of this pathogen in vivo. The host mechanisms involved in this foodborne pathogen shedding are largely unknown. Studies of the transcriptome of recto-anal junction (RAJ) of SS, the primary site of E. coli O157 colonisation[10], revealed lower expression of genes involved in humoral and cell-mediated immune responses[11]. We hypothesis that the difference in physiological functions determined by the transcriptome between small and the large intestine may contribute to the tropism of E. coli O157 colonisation in cattle. The transcriptome profiles of tissues through the whole gastrointestinal tract including duodenum, proximal jejunum, distal jejunum, cecum, spiral colon and descending colon were compared between SS and NS using RNA-Seq and SNP discovery analysis was performed on the identified differentially expressed genes
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