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Surgical Removal of Gut Bacteria Biomass Promotes Weight Gain via Suppression of Energy Expenditure
Author(s) -
Pearson Nicole A,
Riedl Ruth A,
Atkinson Samantha N,
Ollinger Tomye L,
Burnett Colin ML,
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.890.1
Subject(s) - cecum , bacteria , biology , gut flora , feces , energy expenditure , dysbiosis , energy homeostasis , host (biology) , weight gain , energetics , energy balance , physiology , body weight , microbiology and biotechnology , zoology , immunology , endocrinology , ecology , genetics , obesity
A role for gut microbiota in energy homeostasis has been supported by studies involving twins, fecal transplants, colonization of germ‐free animals, and antimicrobial treatments. Although these studies have documented qualitative changes in digestive efficiency and microbiota‐host communication, there have been few attempts to quantitatively assess the relative contributions of these processes. Therefore it remains unclear whether other energy balance mechanisms may also contribute to the observed effects of the gut microbiota upon host energetics. It has been estimated that bacteria contribute 1–3% of adult human body mass, and that bacteria metabolize energy at ~7 kcal/kg/hr; thus bacteria in a 90 kg man should utilize 150–450 kcal/d, which is the equivalent of 7–22% of a 2,000 kcal/d human energy flux. We therefore hypothesize that gut bacteria contribute a physiologically‐relevant fraction of the host's total energy expenditure, and that removal of bacterial biomass would lead to increased weight gain despite simultaneously reducing digestive efficiency. To test this hypothesis we surgically removed the cecum (which is filled with bacteria and accounts for ~1% of body mass in mice) from 13 week old female C57BL/6J mice, and serially assessed host energetics by bomb calorimetry for two months. Compared to sham surgery, cecectomized mice gained significantly more weight (at four weeks: sham n=9, +1.72±0.21 vs cecectomy n=9, +2.95±0.30 g, p<0.05). Animals appeared healthy and active, with no changes in grooming or other behaviors noted. No differences in food (2920x chow) intake behavior (3.54±0.28 vs 3.30±0.12 g/d, p=NS) were observed. As expected, cecectomy significantly reduced digestive efficiency (85.8±1.1 vs 82.4±0.9, p<0.05), but no difference in total caloric absorption was observed (13.71±1.23 vs 12.23±0.50 kcal/d, p=NS). Energy efficiency (weight gain per calorie absorbed) was significantly increased with cecectomy (4.31±0.59 vs 8.15±0.90 mg/kcal, p<0.05). Collectively, these data demonstrate an increase in weight gain after removal of gut bacterial biomass in mice, which occurred due to a major suppression of energy expenditure. Notably the weight gain‐resisting suppression of digestive efficiency was insufficient to offset the reduction in energy expenditure that also occurred with cecectomy, resulting in a net caloric retention and thereby excess weight gain. These data highlight a large, dominant, quantitative contribution of gut bacteria to total energy expenditure. Additional studies to assess the contribution of the gut bacteria to aerobic vs anaerobic energy expenditure are required.