Abstract
Inflammatory bowel diseases (IBD) including Crohn's disease (CD), and ulcerative colitis (UC), are chronic conditions characterized by chronic intestinal inflammation. Adherent invasive Escherichia coli (AIEC) pathotype has been increasingly implicated in the etiopathogenesis of IBD. In a 21-day study, we investigated the effects of AIEC strain UM146 inoculation on microbiota profile of the ileal, cecal, ascending and descending colon in a pig model of experimental colitis. Carrageenan gum (CG) was used to induce colitis in weaner piglets whereas AIEC strain UM146 previously isolated from a CD patient was included to investigate a cause or consequence effect in IBD. Treatments were: (1) control; (2) CG; (3) AIEC strain UM146; and (4) CG+UM146. Pigs in groups 2 and 4 received 1% CG in drinking water from day 1 of the study while pigs in groups 3 and 4 were inoculated with UM146 on day 8. Following euthanization on day 21, tissue mucosal scrapings were collected and used for DNA extraction. The V4 region of bacterial 16S rRNA gene was then subjected to Illumina sequencing. Microbial diversity, composition, and the predicted functional metagenome were determined in addition to short chain fatty acids profiles in the digesta and inflammatory cytokines in the intestinal tissue. CG-induced colitis decreased bacterial species richness and shifted community composition. At the phylum level, an increase in Proteobacteria and Deferribacteres and a decrease in Firmicutes, Actinobacteria, and Bacteroidetes were observed in CG and CGUM146 compared to control and UM146. The metabolic capacity of the microbiome was also altered in CG and CGUM146 compared to UM146 and control in the colon. We demonstrated that CG resulted in bacterial dysbiosis and shifted community composition similar to what has been previously observed in IBD patients. However, AIEC strain UM146 alone did not cause any clear changes compared to CG or control in our experimental IBD pig model.
Highlights
Inflammatory bowel diseases (IBD), including Crohn’s disease (CD), and ulcerative colitis (UC), are a group of inflammatory conditions related to the colon and small intestines and characterized by chronic inflammation
At 48 h post-inoculation, diarrhea was observed in colitic pigs that were inoculated with E. coli (CGUM146 treatment) but not in the other treatment groups (Figure 1A)
In agreement with previous studies in IBD patients (Sokol et al, 2008; Man et al, 2011; Walters et al, 2014; Wright et al, 2015), our results showed that the relative abundance of Proteobacteria was higher (P = 0.001) in pigs with Carrageenan gum (CG)-induced colitis whilst Firmicutes and Bacteroides were lower (P < 0.001) compared to control in the large intestine (Figure 3, Supplementary Table 1)
Summary
Inflammatory bowel diseases (IBD), including Crohn’s disease (CD), and ulcerative colitis (UC), are a group of inflammatory conditions related to the colon and small intestines and characterized by chronic inflammation. Abnormal shifts in the intestinal microbiota, termed dysbiosis, may lead to adverse health effects in the host, and could be critical in the pathogenesis and severity of IBD (Manichanh et al, 2006; Frank et al, 2007; Honda and Littman, 2012; Morgan et al, 2012; Fite et al, 2013) In this context, mice genetically modified for IBD do not develop colitis under germ-free conditions (Horwitz, 2007; Vijay-Kumar et al, 2007, 2010), and the therapeutic effect of antibiotics further supports bacterial contribution in the pathogenesis of IBD (Chapman et al, 1986; van Kruiningen, 1995; Vijay-Kumar et al, 2010). The breakdown in the balance between “mutualistic and commensal” vs. “opportunistic and pathogenic” intestinal bacteria, largely characterized by reduced abundance of members of Firmicutes, Actinobacteria, and Bacteroidetes, and an increase in Proteobacteria and in some cases Bacteroidetes, is suggested to promote chronic intestinal inflammation (Sokol et al, 2008; Man et al, 2011; Walters et al, 2014; Wright et al, 2015)
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