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The Biomass and Composition of the Gut Microbiota Modify Anaerobic Metabolism
Author(s) -
Riedl Ruth A,
Burnett Colin ML,
Pearson Nicole A,
Atkinson Samantha N,
Ollinger Tomye L,
Edwards Robert A,
Mokadem Mohamad,
Kirby John R,
Grobe Justin L
Publication year - 2017
Publication title -
the faseb journal
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.709
H-Index - 277
eISSN - 1530-6860
pISSN - 0892-6638
DOI - 10.1096/fasebj.31.1_supplement.890.2
Subject(s) - cecum , anaerobic exercise , anaerobic bacteria , gut flora , prevotella , respirometry , zoology , biology , fusobacterium , caecum , basal metabolic rate , metabolism , chemistry , bacteria , microbiology and biotechnology , medicine , food science , physiology , endocrinology , biochemistry , bacteroides , ecology , genetics
The lumen of the gastrointestinal tract is host to a large mass of microbiota, and this environment is largely anaerobic. Previous studies have estimated that bacteria contribute 1–3% (~1–3 kg) of an adult human's body mass and that bacteria typically exhibit an ~7 kcal/kg/hr metabolic rate, which implies a total contribution of 150–450 kcal/d to the host's apparent energy expenditure. Surprisingly, however, few studies have attempted to directly quantify the metabolic rate of the gut microbiota in the in vivo setting. We hypothesized that the biomass and composition of the bacterial community would both contribute to the metabolic rate of the gut microbiota, and that the energy flux through this biomass would be anaerobic in nature. Total resting metabolic rate (tRMR) was assessed using direct calorimetry; aerobic (aRMR) was determined using respirometry, and anaerobic RMR (anRMR) was determined as the difference in results between the two methods. Wildtype C57BL/6J mice were anesthetized with ketamine/xylazine to measure baseline tRMR, and tRMR after surgical removal of the cecum. A subset of animals was also pre‐treated with risperidone. Surgical removal of the cecum, which accounts for ~1% of body mass in mice, resulted in an 8% reduction in tRMR within minutes of surgery (sham n=12 pre 0.116±0.004; cecectomy n=13 pre 0.115±0.004; sham post 0.113±0.004; cecectomy post 0.104±0.005 p<0.05 vs pre, in kcal/hr). Pre‐treatment with risperidone (which we have previously demonstrated to have major modulatory effects upon the composition of the gut microbiome) suppressed tRMR (n=14 pre 0.104±0.004, p<0.05 vs sham pre), and cecectomy in pretreated mice had no additive effect to suppress tRMR (post 0.099±0.004). These results demonstrate that removal of gut microbiota reduces tRMR, subject to the composition of the bacterial community. Next, a cohort of overweight C57BL/6J mice underwent Roux‐en‐Y gastric bypass (RYGB) or sham surgery. After one week, tRMR was significantly increased by 10% in the RYGB group (sham n=8, 0.141±0.003 vs RYGB n=10, 0.154±0.003 kcal/hr, p<0.05) while aRMR remained unchanged (0.140±0.003 vs 0.143±0.003 kcal/hr, p=NS), indicating that the increase in tRMR was completely due to an increase in anRMR (0.001±0.003 vs 0.011±0.003 kcal/hr, p<0.05). These results demonstrate that increased biomass of gut bacteria via RYGB surgery is associated with an increase in energy expenditure, specifically in the form of anRMR. Collectively these data highlight a major contribution of gut microbiota to total energy expenditure in mice, and support the general concept that the energy flux through this biomass is anaerobic and subject to the composition of the bacterial community present.