Alterations in the Colonic Microbiota in Response to Osmotic Diarrhea

Gorkiewicz, Gregor; Thallinger, Gerhard G.; Trajanoski, Slave; Lackner, Sonja; Stocker, Gernot; Hinterleitner, Thomas; Gülly, Christian; Högenauer, Christoph

doi:10.1371/journal.pone.0055817

Cited by 111 publications

(99 citation statements)

References 78 publications

(89 reference statements)

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“…In humans, osmotic diarrhea from oral ingestion of polyethylene glycol was found in general to increase Firmicutes members in the stool and decrease Bacteroidetes members in the mucosa-associated bacterial population. Moreover, diarrhea led to a relative increase in the abundance of Proteobacteria (33). The data herein demonstrate that NHE3 Ϫ/Ϫ mice have increased Bacteroidetes and decreased Firmicutes phyla both in the luminal and mucosa-associated bacterial populations.…”

Section: Discussionmentioning

confidence: 51%

Loss of NHE3 alters gut microbiota composition and influencesBacteroides thetaiotaomicrongrowth

Engevik

Aihara

Montrose

et al. 2013

American Journal of Physiology-Gastrointestinal and Liver Physi

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Changes in the intestinal microbiota have been linked to diabetes, obesity, inflammatory bowel disease, and Clostridium difficile ( C. difficile)-associated disease. Despite this, it remains unclear how the intestinal environment, set by ion transport, affects luminal and mucosa-associated bacterial composition. Na+/H+-exchanger isoform 3 (NHE3), a target of C. difficile toxin B, plays an integral role in intestinal Na+ absorption. Thus the NHE3-deficient mouse model was chosen to examine the effect of pH and ion composition on bacterial growth. We hypothesized that ion transport-induced change in the intestinal environment would lead to alteration of the microbiota. Region-specific changes in ion composition and pH correlated with region-specific alteration of luminal and mucosal-associated bacteria with general decreases in Firmicutes and increases in Bacteroidetes members. Bacteroides thetaiotaomicron ( B. thetaiotaomicron) increased in NHE3−/− terminal ileum and was examined in vitro to determine whether altered Na+ was sufficient to affect growth. Increased in vitro growth of B. thetaiotaomicron occurred in 43 mM Na+ correlating with the NHE3−/− mouse terminal ileum [Na+]. NHE3−/− terminal ileum displayed increased fut2 mRNA and fucosylation correlating with B. thetaiotaomicron growth. Inoculation of B. thetaiotaomicron in wild-type and NHE3−/− terminal ileum organoids displayed increased fut2 and fucosylation, indicating that B. thetaiotaomicron alone is sufficient for the increased fucosylation seen in vivo. These data demonstrate that loss of NHE3 alters the intestinal environment, leading to region-specific changes in bacteria, and shed light on the growth requirements of some gut microbiota members, which is vital for creating better treatments of complex diseases with an altered gut microbiota.

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Section: Discussionmentioning

confidence: 51%

Loss of NHE3 alters gut microbiota composition and influencesBacteroides thetaiotaomicrongrowth

Engevik

Aihara

Montrose

et al. 2013

American Journal of Physiology-Gastrointestinal and Liver Physi

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“…Fecal microbe-metabolite associations in health and IBS V Shankar et al collection, and there was only a small difference in the average water content of the collected stool samples between healthy and IBS-D groups, both diet changes and diarrhea have been shown to cause alterations in human gut microbiota (David et al, 2014, Gorkiewicz et al, 2013. Thus, some of the observed IBS-associated effects on the gut environment might be manifestations of the concurrent changes in eating and bowel evacuation patterns in individuals with IBS-D.…”

Section: Discussionmentioning

confidence: 99%

The networks of human gut microbe–metabolite associations are different between health and irritable bowel syndrome

et al. 2015

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The goal of this study was to determine if fecal metabolite and microbiota profiles can serve as biomarkers of human intestinal diseases, and to uncover possible gut microbe-metabolite associations. We employed proton nuclear magnetic resonance to measure fecal metabolites of healthy children and those diagnosed with diarrhea-predominant irritable bowel syndrome (IBS-D). Metabolite levels were associated with fecal microbial abundances. Using several ordination techniques, healthy and irritable bowel syndrome (IBS) samples could be distinguished based on the metabolite profiles of fecal samples, and such partitioning was congruent with the microbiota-based sample separation. Measurements of individual metabolites indicated that the intestinal environment in IBS-D was characterized by increased proteolysis, incomplete anaerobic fermentation and possible change in methane production. By correlating metabolite levels with abundances of microbial genera, a number of statistically significant metabolite-genus associations were detected in stools of healthy children. No such associations were evident for IBS children. This finding complemented the previously observed reduction in the number of microbe-microbe associations in the distal gut of the same cohort of IBS-D children.

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“…These observations are consistent with previous studies describing osmotic diarrhea involving the colon. In those studies, increased osmotic pressure in the colon from other agents induced diarrhea, with this effect comprising the basis for several commonly used laxatives (32)(33)(34)(35).…”

Section: Figmentioning

confidence: 99%

Clostridium perfringens Type A Enterotoxin Damages the Rabbit Colon

García

Shrestha

et al. 2014

Infect Immun

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bClostridium perfringens enterotoxin causes the gastrointestinal (GI) symptoms of C. perfringens type A food poisoning and CPE-associated non-food-borne human GI diseases. It is well established that CPE induces fluid accumulation and severe tissue damage in ligated small intestinal loops of rabbits and other animals. However, a previous study had also reported that CPE binds to rabbit colonic cells yet does not significantly affect rabbit colonic loops. To the contrary, the current study determined that treatment with 50 or 100 g/ml of CPE causes significant histologic lesions and luminal fluid accumulation in rabbit colonic loops. Interestingly, a CPE-neutralizing monoclonal antibody blocked the development of CPE-induced histologic damage but not luminal fluid accumulation in these loops. Similar luminal fluid accumulation, without significant histologic damage, also occurred after treatment of colonic loops with heat-inactivated CPE, antibody alone, or bovine serum albumin (BSA), indicating that increased osmolarity was causing or contributing to fluid accumulation in CPE-treated colonic loops. Comparative studies revealed the similar development of histologic damage and luminal fluid accumulation in both small intestinal loops and colonic loops after as little as a 1-h treatment with 50 g/ml of CPE. Consistent with the CPE sensitivity of the small intestine and colon, Western blotting detected CPE binding and large-complex formation in both organs. In addition, Western blotting demonstrated the presence of the high-affinity CPE receptors claudin-3 and -4 in both organs of rabbits, consistent with the observed toxin binding. Collectively, these results offer support for the possible involvement of the colon in CPE-mediated GI disease.

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Alterations in the Colonic Microbiota in Response to Osmotic Diarrhea

Cited by 111 publications

References 78 publications

Loss of NHE3 alters gut microbiota composition and influencesBacteroides thetaiotaomicrongrowth

Loss of NHE3 alters gut microbiota composition and influencesBacteroides thetaiotaomicrongrowth

The networks of human gut microbe–metabolite associations are different between health and irritable bowel syndrome

Clostridium perfringens Type A Enterotoxin Damages the Rabbit Colon

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