Environmental pollutant-mediated disruption of gut microbial metabolism of the prebiotic inulin

Authors: HOFFMAN, JESSIE - University Of Kentucky; Flythe, Michael; HENNIG, BERNHARD - University Of Kentucky

Submitted to: Anaerobe
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/14/2018
Publication Date: N/A
Citation: N/A

Interpretive Summary: Environmental pollutant exposure is a global problem that increases an individual’s risk of disease development including cardiovascular disease and diabetes. Since a common route of exposure to persistent organic pollutants is through contaminated foods, examining the impact that exposure exerts on the gut microbiota is important. The objective of this study was to examine the impacts of pollutant exposure, specifically polychlorinated biphenyl PCB 126, on gut bacteria and their ability to fermentation the prebiotic dietary fiber, inulin. Exposure to PCB 126 decreased viability of an inulin-utilizing bacterium that was isolated from an inulin-fed mouse. It appeared that PCB 126 could damage the membrane that surrounds the bacterial cell. Furthermore, PCB 126 exposure altered inulin fermentation and acid production by mixed mouse gut microorganisms. This result showed that the pollutant effected the gut microbiota as a whole, not just the individual isolated bacterium. The pollutant induced reductions in succinate and increases in propionate, which could be important because these two fermentation acids contribute to glucose and lipid metabolism in the host. This research suggests that pollutant exposure may contribute to disruptions in host metabolism through gut microbial fermentation. The impact of this research is that environmental pollutants could adversely affect gastrointestinal microbiology, functional fiber utilization and, consequently, the health of both humans and animals.

Technical Abstract: Exposure to environmental pollutants is associated with a greater risk for metabolic diseases, including cardiovascular disease. Pollutant exposure can also alter gut microbial populations that may contribute to metabolic effects and progression of inflammatory diseases. Short-chain fatty acids (SCFAs), produced from gut fermentation of dietary carbohydrates, such as inulin, exert numerous effects on host energy metabolism. SCFAs are also linked to health promoting effects, including a reduced risk of inflammatory diseases. The hypothesis was that exposure to dioxin-like pollutants modulate gut microbial fermentation processes. Fecal microbes from mice were harvested, suspended and incubated in anaerobic media containing inulin with or without PCB 126. HPLC analysis revealed that PCB 126 exposure changed the production of several SCFA, including succinic- and propionic-acid. Exposure to PCB 126 reduced succinic acid production, while exposure to higher levels of PCB 126 increased total fermentation acids, in particular propionate production. It has been demonstrated that bacteria-produced succinate contributes to metabolic benefits by acting as an intestinal gluconeogenic substrate. Furthermore, there is evidence that excess propionate and total SCFA can contribute to increased energy harvest and hepatic lipogenesis. To examine the possible mechanisms of the observed modulation of SCFA production we next examined the effects of PCBs on bacterial membrane integrity and/or metabolism by quantifying changes in intracellular potassium. Upon exposure to PCB 126, bacterial cells lost intracellular potassium while control continued to accumulate intracellular potassium. These results indicate that PCB 126 either disrupts the cell membrane of certain bacteria. Overall, the presented evidence supports the idea that pollutant exposure can contribute to alterations in host metabolism through gut microbiota-dependent mechanisms, specifically through bacterial fermentation processes or membrane disruption.