Bromochloromethane, a Methane Analogue, Affects the Microbiota and Metabolic Profiles of the Rat Gastrointestinal Tract

Abstract

Bromochloromethane (BCM), an inhibitor of methanogenesis, has been used in animal production. However, little is known about its impact on the intestinal microbiota and metabolic patterns. The present study aimed to investigate the effect of BCM on the colonic bacterial community and metabolism by establishing a Wistar rat model. Twenty male Wistar rats were randomly divided into two groups (control and treated with BCM) and raised for 6 weeks. Bacterial fermentation products in the cecum were determined, and colonic methanogens and sulfate-reducing bacteria (SRB) were quantified. The colonic microbiota was analyzed by pyrosequencing of the 16S rRNA genes, and metabolites were profiled by gas chromatography and mass spectrometry. The results showed that BCM did not affect body weight and feed intake, but it did significantly change the intestinal metabolic profiles. Cecal protein fermentation was enhanced by BCM, as methylamine, putrescine, phenylethylamine, tyramine, and skatole were significantly increased. Colonic fatty acid and carbohydrate concentrations were significantly decreased, indicating the perturbation of lipid and carbohydrate metabolism by BCM. BCM treatment decreased the abundance of methanogen populations, while SRB were increased in the colon. BCM did not affect the total colonic bacterial counts but significantly altered the bacterial community composition by decreasing the abundance of actinobacteria, acidobacteria, and proteobacteria. The results demonstrated that BCM treatment significantly altered the microbiotic and metabolite profiles in the intestines, which may provide further information on the use of BCM in animal production. Bromochloromethane (BCM) (CH 2 BrCl, CAS no. 74-97-5) is an analog of dihalogenated methane. Unintentional consumption of this unregulated halomethane as a by-product of disinfection in drinking water is one of the major sources for BCM exposure (1, 2) and has been linked to an increased risk of stomach cancer in Finland (3). Long-term exposure to BCM may cause hepato-and nephrotoxicity in humans. Budnik et al. (4) reviewed 542 publications between 1990 and 2011 and found 91 publications referring to the toxicity of halomethanes on lungs, skin, liver, muscle, spleen, kidneys, and the central nervous system. Although the gastrointestinal tract (GIT) comes in direct contact with ingested BCM, very few studies have focused on the influence of BCM on the GIT, let alone on the intestinal microbiota.BCM can be used as an antimethanogenic compound to decrease methane production. BCM supplementation at 0.3 g/100 kg of body weight (BW) significantly decreased methane production and methanogen abundance in Japanese goats (5), lactating dairy goats (6), steers (7), and Sprague-Dawley (SD) rats (8). BCM inhibits methanogenesis by reacting with cobalamin (9). Cobalamin-dependent enzymes, including cobalamin-dependent methionine synthase (10), methylmalonyl-coenzyme A (CoA) mutase, and glutamate mutase, contribute to the bacterial metabolism under physiological conditions. ...

The gut microbiota is largely independent of host genetics in regulating fat deposition in chickens

“…Gordon et al [21] revealed that the co-inoculation of gnotobiotic mice with M. smithii and the polysaccharidefermenting bacterium B. thetaiotaomicron significantly increased the amounts of caecal fermentation products (such as acetate, propionate and butyrate), total liver triglycerides and host fat stores without affecting the total BW. Several previous studies showed that antimethanogenic compounds (such as bromochloromethane) could effectively decrease the abundance of methanogen populations and have no effect on BW [89,90]. In addition, our results demonstrated that Methanobrevibacter had limited association with other gut microbiota and was not influenced by host genetic regulation.…”

Review: Comparative methane production in mammalian herbivores

“…In mice, the presence of methanogens led to a more efficient carbohydrate digestion and higher body fat stores (but not higher BM) at similar food intakes, compared to animals without methanogens or those inoculated with a sulphate-reducing bacterium as an alternative H 2 sink (Samuel and Gordon, 2006). In rats, reducing methanogens led to a less efficient use of carbohydrates, but no change in BM over 6 weeks (Yang et al, 2016). Reducing methanogens/CH 4 emissions in humans has been associated with a decrease in digesta retention (Ghoshal et al, 2018).…”

Response of Gut Microbiota to Dietary Fiber and Metabolic Interaction With SCFAs in Piglets

“…Soil DNA Kit (Omega Bio-tek, Norcross, GA, United States) according to manufacturer’s protocols. The final DNA concentration and purity were determined by NanoDrop 2000 UV–vis spectrophotometer (Thermo Scientific, Wilmington, NC, United States), and DNA quality was checked by 1% agarose gel electrophoresis ( Yang et al, 2015 ). The V3–V4 hypervariable regions of the bacterial 16S rRNA gene were amplified with primers 338F (5′-ACTCCTACGGGAGGCAGCAG-3′) and 806R (5′-GGACTACHVGGGTWTCTAAT-3′) by PCR (GeneAmp 9700, ABI, United States; Singh et al, 2015 ) using the following program: 3 min denaturation at 95°C; 27 cycles of 30 s at 95°C, 30 s annealing at 55°C, and 45 s elongation at 72°C; and a final extension at 72°C for 10 min.…”