Chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome

Abstract

Background Salmonella is one of the most significant food-borne pathogens to affect humans and agriculture. While it is well documented that Salmonella infection triggers host inflammation, the impacts on the gut environment are largely unknown. A CBA/J mouse model was used to evaluate intestinal responses to Salmonella-induced inflammation. In parallel, we evaluated chemically induced inflammation by dextran sodium sulfate (DSS) and a non-inflammation control. We profiled gut microbial diversity by sequencing 16S ribosomal ribonucleic acid (rRNA) genes from fecal and cecal samples. These data were correlated to the inflammation marker lipocalin-2 and short-chain fatty acid concentrations.ResultsWe demonstrated that inflammation, chemically or biologically induced, restructures the chemical and microbial environment of the gut over a 16-day period. We observed that the ten mice within the Salmonella treatment group had a variable Salmonella relative abundance, with three high responding mice dominated by >46% Salmonella at later time points and the remaining seven mice denoted as low responders. These low- and high-responding Salmonella groups, along with the chemical DSS treatment, established an inflammation gradient with chemical and low levels of Salmonella having at least 3 log-fold lower lipocalin-2 concentration than the high-responding Salmonella mice. Total short-chain fatty acid and individual butyrate concentrations each negatively correlated with inflammation levels. Microbial communities were also structured along this inflammation gradient. Low levels of inflammation, regardless of chemical or biological induction, enriched for Akkermansia spp. in the Verrucomicrobiaceae and members of the Bacteroidetes family S24-7. Relative to the control or low inflammation groups, high levels of Salmonella drastically decreased the overall microbial diversity, specifically driven by the reduction of Alistipes and Lachnospiraceae in the Bacteroidetes and Firmicutes phyla, respectively. Conversely, members of the Enterobacteriaceae and Lactobacillus were positively correlated to high levels of Salmonella-induced inflammation.ConclusionsOur results show that enteropathogenic infection and intestinal inflammation are interrelated factors modulating gut homeostasis. These findings may prove informative with regard to prophylactic or therapeutic strategies to prevent disruption of microbial communities, or promote their restoration.Electronic supplementary materialThe online version of this article (doi:10.1186/s40168-017-0264-8) contains supplementary material, which is available to authorized users.

Astrovirus infections induce age-dependent dysbiosis in gut microbiomes of bats

“…Analogously, both Lachnospiraceae (OTU4155396) and Ruminococcaceae (OTU11308) showed negative relationships with Peptostreptococcaceae (OTU351976). This is in accordance with previous findings that members from both Lachnospiraceae and Ruminococcaceae exhibit negative interactions with invading pathogens [56], are important components of gut health and their loss can result in diarrhoea [44]. Similarly, in adult bats, we observed a negative interaction of a potential pathogenic member of Streptococcus (OTU1141646) with Xanthomonadaceae (OTU548694, OTU3055791) and Enterobacteriaceae (OTU746679) and, likewise, of Peptostreptococcaceae (OTU308309) with Enterobacteriaceae (OTU211).…”

Probiotic Mixture of Lactobacillus plantarum Strains Improves Lipid Metabolism and Gut Microbiota Structure in High Fat Diet-Fed Mice

“…Bifidobacterium, a beneficial microbial species, producing lactic acid and acetic acid, can reduce intestinal pH and inhibit the growth of various detrimental bacteria to maintain intestinal health (Wang R. et al, 2018). Bacteroides, Alistipes, Lachnospiraceae NK4A136 group and Alloprevotella are also capable of producing SCFAs such as acetic acid and butyric acid (Borton et al, 2017;Gotoh et al, 2017;Jiang et al, 2018;Yin et al, 2018). It was reported that the abundance of Bacteroides was reduced in individuals with atherosclerotic cardiovascular disease (Jie et al, 2017) and post-inflammatory irritable bowel syndrome .…”

The reduction of DSS-induced colitis severity in mice exposed to cigarette smoke is linked to immune modulation and microbial shifts

“…Akkermansia is substantially reduced in the mucosal tissues of CD and UC patients 77 , and its abundance is inversely correlated with the onset of inflammation in metabolic diseases 29 . Further support for the beneficial effects of Akkermansia on colitis is derived from the observation that Akkermansia extracellular vesicles protect against DSS-induced colitis 78 and from Akkermansia's ability to produce propionate 79 ,a possible anti-inflammatory agent in the gut 80 . Nonetheless, several publications have reported increased Akkermansia abundance in mice following DSS treatment 27,61,79 .…”

“…Further support for the beneficial effects of Akkermansia on colitis is derived from the observation that Akkermansia extracellular vesicles protect against DSS-induced colitis 78 and from Akkermansia's ability to produce propionate 79 ,a possible anti-inflammatory agent in the gut 80 . Nonetheless, several publications have reported increased Akkermansia abundance in mice following DSS treatment 27,61,79 . The varying effects of inflammation on mucin expression and mucus production may explain these contradictory findings.…”

“…The varying effects of inflammation on mucin expression and mucus production may explain these contradictory findings. Regardless of the causative agent, lower levels of inflammation stimulate mucin production, while high levels inhibit it 79 . In our model, the expression of several mucin genes was consistently upregulated by DSS treatment, explaining the increase in Akkermansia in the DSS-treated group that was not exposed to CS.…”