Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models
- E F Murphy1,2,
- P D Cotter1,3,
- S Healy2,
- T M Marques1,3,
- O O'Sullivan1,3,
- F Fouhy3,
- S F Clarke3,4,
- P W O'Toole1,4,
- E M Quigley1,
- C Stanton1,3,
- P R Ross1,3,
- R M O'Doherty1,5,6,
- F Shanahan1
- 1Alimentary Pharmabiotic Centre, University College Cork, Ireland
- 2Alimentary Health Ltd, Cork, Ireland
- 3Teagasc Moorepark Food Research Centre, Fermoy, County Cork, Ireland
- 4Department of Microbiology, University College Cork, Ireland
- 5Department of Medicine, Division of Endocrinology and Metabolism, University of Pittsburgh, Pittsburgh, USA
- 6Department of Microbiology and Molecular Genetics, University of Pittsburgh, Pittsburgh, USA
- Correspondence to Professor Fergus Shanahan, Department of Medicine and Alimentary Pharmabiotic Centre, University College Cork, National University of Ireland, Cork, Ireland;
Contributors EFM, PDC, FS, EMQ, CS, PRR, PWOT and RMOD were involved in study design and concept; EFM, SH, TMM, FF, SC, OO'S and PDC were involved in acquisition and analysis of the data; EFM, FS and PDC were involved in drafting the manuscript; EFM, PDC, FS, EMQ, CS, PRR, PWOT and RMOD were involved in revision of the manuscript.
- Accepted 15 July 2010
- Published Online First 6 October 2010
Background and Aims Increased efficiency of energy harvest, due to alterations in the gut microbiota (increased Firmicutes and decreased Bacteroidetes), has been implicated in obesity in mice and humans. However, a causal relationship is unproven and contributory variables include diet, genetics and age. Therefore, we explored the effect of a high-fat (HF) diet and genetically determined obesity (ob/ob) for changes in microbiota and energy harvesting capacity over time.
Methods Seven-week-old male ob/ob mice were fed a low-fat diet and wild-type mice were fed either a low-fat diet or a HF-diet for 8 weeks (n=8/group). They were assessed at 7, 11 and 15 weeks of age for: fat and lean body mass (by NMR); faecal and caecal short-chain fatty acids (SCFA, by gas chromatography); faecal energy content (by bomb calorimetry) and microbial composition (by metagenomic pyrosequencing).
Results A progressive increase in Firmicutes was confirmed in both HF-fed and ob/ob mice reaching statistical significance in the former, but this phylum was unchanged over time in the lean controls. Reductions in Bacteroidetes were also found in ob/ob mice. However, changes in the microbiota were dissociated from markers of energy harvest. Thus, although the faecal energy in the ob/ob mice was significantly decreased at 7 weeks, and caecal SCFA increased, these did not persist and faecal acetate diminished over time in both ob/ob and HF-fed mice, but not in lean controls. Furthermore, the proportion of the major phyla did not correlate with energy harvest markers.
Conclusion The relationship between the microbial composition and energy harvesting capacity is more complex than previously considered. While compositional changes in the faecal microbiota were confirmed, this was primarily a feature of high-fat feeding rather than genetically induced obesity. In addition, changes in the proportions of the major phyla were unrelated to markers of energy harvest which changed over time. The possibility of microbial adaptation to diet and time should be considered in future studies.
- mouse models
- bacterial interactions
- nutrient absorption
- small intestine
Linked articles 223594.
Funding The authors are supported in part by Teagasc (an Agency of the Irish Government Department of Agriculture, Fisheries and Food), by Science Foundation Ireland (in the form of a research centre grant to the Alimentary Pharmabiotic Centre and a PI award to PWOT), by Grant NIH RO1 DK058855 (to RMOD) and by Alimentary Health Ltd.
Competing interests None.
Ethics approval All animal experiments were approved by the UCC Animal Ethics Committee and experimental procedures were conducted under appropriate licence from the Irish government.
Provenance and peer review Not commissioned; externally peer reviewed.