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High-Fat Diet Determines the Composition of the Murine Gut Microbiome Independently of Obesity
Open accessAbstract
Background & aims The composition of the gut microbiome is affected by host phenotype, genotype, immune function, and diet. Here, we used the phenotype of RELMbeta knockout (KO) mice to assess the influence of these factors.Methods Both wild-type and RELMbeta KO mice were lean on a standard chow diet, but, upon switching to a high-fat diet, wild-type mice became obese, whereas RELMbeta KO mice remained comparatively lean. To investigate the influence of diet, genotype, and obesity on microbiome composition, we used deep sequencing to characterize 25,790 16S rDNA sequences from uncultured bacterial communities from both genotypes on both diets.Results We found large alterations associated with switching to the high-fat diet, including a decrease in Bacteroidetes and an increase in both Firmicutes and Proteobacteria. This was seen for both genotypes (ie, in the presence and absence of obesity), indicating that the high-fat diet itself, and not the obese state, mainly accounted for the observed changes in the gut microbiota. The RELMbeta genotype also modestly influenced microbiome composition independently of diet. Metagenomic analysis of 537,604 sequence reads documented extensive changes in gene content because of a high-fat diet, including an increase in transporters and 2-component sensor responders as well as a general decrease in metabolic genes. Unexpectedly, we found a substantial amount of murine DNA in our samples that increased in proportion on a high-fat diet.Conclusions These results demonstrate the importance of diet as a determinant of gut microbiome composition and suggest the need to control for dietary variation when evaluating the composition of the human gut microbiome.
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“administration of an HFD to healthy subjects caused a decrease in Bacteroidetes levels with an increase in both Firmicutes and Proteobacteria levels of gut microbiota (Hildebrandt et al., 2009;Zhang et al., 2012a).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Hildebrandt et al., 2009
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“animal models fed an HFD demonstrated an alteration in their gut microbiota profile with a reduction in Bacteroidetes levels and an increase in both Proteobacteria and Firmicute levels (Hildebrandt et al., 2009).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Hildebrandt et al., 2009
In the citing paper
“Those with cystic fibrosis are recommended to consume a diet high in protein and fat (and therefore a comparative reduction in carbohydrates) which has been previously associated with an increase in Firmicutes to Bacteriodetes ratio in mice [96], though dietary data was not collected within the cystic fibrosis study [95].”
From Effect of Diet on the Gut Microbiota: Rethinking Intervention Duration (2019) · cites this paper as [96]
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“These changes were observed in mice resistant to weight gain, implying a direct effect of dietary lipids on the microbiota (26, 27).”
From The gut microbiota at the intersection of diet and human health (2018) · cites this paper as [26]
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“Experimental mice fed a high-fat diet (40 to 80% total caloric intake) exhibit decreases at the phyla-level in Bacteroidetes and increases in Firmicutes and Proteobacteria.”
From The gut microbiota at the intersection of diet and human health (2018) · cites this paper as [26]
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“a high-fat diet, independent of obesity, altered the composition of the intestinal microbiome (Hildebrandt, 2009).”
From Viral Infections, the Microbiome, and Probiotics (2021) · cites this paper as Hildebrandt, 2009
In the citing paper
“Similar to the Western diet, high-fat diets in animal studies reproducibly change gut microbial community structure, decreasing the overall microbiota diversity and beneficial bacteria (e.g., A. muciniphila, Bifidobacterium, Lactobacillus, and Lactococcus) and increasing the Firmicutes:Bacteroidetes ratio and the abundance of Enterobacteriales, Clostridium cluster XVIa, Mollicutes, and B. wadswort”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [90]
In the citing paper
“To further isolate the solitary impact of sleep on the microbiota – separate from the previously documented impact of e.g. high-fat diet [32] – participants were provided with a non-sugar sweetened, low-fat diet throughout the three meals, the exception being the oral glucose tolerance (OGTT) test on day 2”
From Gut microbiota and glucometabolic alterations in response to recurrent partial sleep deprivation in normal-weight young individuals (2016) · cites this paper as [32]
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“Consistent with previous reports [20,31], the gut microbiome derived from HFD-fed donors (HF-D) contained an increased fraction of Firmicutes and lower levels of Bacteroidetes as compared to CC-fed donors (CC-D) (Fig EV1A).”
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Direct sequencing of the human microbiome readily reveals community differences
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Role of Gut Dysbiosis in Liver Diseases: What Have We Learned So Far?
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“Although both genotypes showed extensive changes in gut microbiome including a decrease in Bacteroidetes and an increase in both Firmicutes and Proteobacteria, RELMβ KO mice remain comparatively lean on a high-fat diet, indicating that the high-fat diet and not the obese state, predisposes to the dysbiosis [79].”
BackgroundHaro, C., García‐Carpintero, S., Rangel‐Zúñiga, O. A., Alcalá‐Díaz, J. F., Landa, B. B., Clemente, J. C., Pérez‐Martínez, P., López‐Miranda, J., Pérez‐Jiménez, F., & Camargo, A. (2017) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201700300 · Cited by 149
The Gordian Knot of dysbiosis, obesity and NAFLD
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Linking microbiota to human diseases: a systems biology perspective
Wu, H., Tremaroli, V., & Bäckhed, F. (2015) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2015.09.011 · Cited by 150
“The gut microbiota responds rapidly to dietary interventions [45–47] and short-term consumption of diets comprising entirely either animal or plant products can alter the overall structure of the gut microbiota [45].”
BackgroundPathophysiological role of host microbiota in the development of obesity
Kobyliak, N. M., Virchenko, O., & Falalyeyeva, T. M. (2015) · Nutrition Journal · doi:10.1186/s12937-016-0166-9 · Cited by 156
“Several studies have confirmed this interaction, including a recent one showing that TM-IEC C1galt(-/-) mice with altered intestinal architecture have impaired gut microbiota composition with inverse shifts in the abundance of the phyla Bacteroidetes and Firmicutes.”
BackgroundInfluentialTang, W., Yao, X., Xia, F., Yang, M., Chen, Z., Zhou, B., & Liu, Q. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/7261619 · Cited by 151
Impact of the Gut Microbiota on the Development of Obesity: Current Concepts
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“In a recent study on the effects of a high fat diet on the gut microbiota, Hildebrandt et al show that in switching lean mice to a HF diet, there was the expected decrease in Bacteriodetes and an increase in Firmicutes and Proteobacteria [42].”
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“[34] observed changes in gut microbiota with a high-fat diet regardless of whether the mice were lean or obese.”
BackgroundNon-nutritive sweeteners possess a bacteriostatic effect and alter gut microbiota in mice
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Microbiota‐gut‐brain axis as a regulator of reward processes
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“An increase in energy consumption above the optimal levels for the individual can provide an excess of substrates that favour the explosive growth of certain microbial populations to the detriment of others (Hildebrandt et al., 2009; Ierardi et al., 2016; Lin et al., 2019; Tomas et al., 2016).”
BackgroundKrebs, N. F., Sherlock, L. G., Westcott, J., Culbertson, D., Hambidge, K. M., Feazel, L. M., Robertson, C. E., & Frank, D. N. (2013) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2013.01.024 · Cited by 149
Microbiota Features Associated With a High-Fat/Low-Fiber Diet in Healthy Adults
Bailén, M., Bressa, C., Martínez‐López, S., González-Soltero, R., Montalvo-Lominchar, M. G., Juan, C. S., & Larrosa, M. (2020) · Frontiers in Nutrition · doi:10.3389/fnut.2020.583608 · Cited by 152
Microbial Regulation of Glucose Metabolism and Cell-Cycle Progression in Mammalian Colonocytes
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“Bacteroidetes and Proteobacteria [141–143].”
Diet, microbes, and host genetics: the perfect storm in inflammatory bowel diseases
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“perspective, that have been shown to play a role in complex disorders such as IBD in both human and animal studies [10–16].”
BackgroundDysbiosis, malnutrition and enhanced gut-lung axis contribute to age-related respiratory diseases
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Gut Microbiota in Obesity and Undernutrition
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Use of dietary indices to control for diet in human gut microbiota studies
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Hepatitis C Virus Transmission Bottlenecks Analyzed by Deep Sequencing
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Self-citationHigh-Fat Diet Changes Fungal Microbiomes and Interkingdom Relationships in the Murine Gut
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“Emerging evidence demonstrates that diet, both independently and in conjunction with body composition, modulates gut microbial community structure (1, 2).”
BackgroundMechanistic links between gut microbial community dynamics, microbial functions and metabolic health
Ha, C. W. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i44.16498 · Cited by 137
Habitual Dietary Intake Is Associated with Stool Microbiota Composition in Monozygotic Twins
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“(36), administration of a high-fat diet to both wild-type and RELMb knockout mice, resistant to fat-induced obesity, increased the relative proportions of the phyla Proteobacteria, Firmicutes, and Actinobacteria in the feces, whereas the levels of Bacteroidetes decreased in both mice.”
BackgroundFaecal microbiota in lean and obese dogs
Handl, S., German, A. J., Holden, S. L., Dowd, S. E., Steiner, J. M., Heilmann, R. M., Grant, R. W., Swanson, K. S., & Suchodolski, J. S. (2013) · FEMS Microbiology Ecology · doi:10.1111/1574-6941.12067 · Cited by 137
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“Dietary changes affect both the structure and function of the gut microbiome in animals (Hildebrandt et al., 2009), and humans under controlled feeding conditions (Wu et al., 2011).”
Metagenomic assessment of the functional potential of the rumen microbiome in Holstein dairy cows
Pitta, D., Indugu, N., Kumar, S., Vecchiarelli, B., Sinha, R., Baker, L. D., Bhukya, B., & Ferguson, J. D. (2015) · Anaerobe · doi:10.1016/j.anaerobe.2015.12.003 · Cited by 138
It's the fiber, not the fat: significant effects of dietary challenge on the gut microbiome
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“Similar changes to gut microbiota have been previously reported in mice consuming a rHFD, suggesting that the bloom of Clostridia and Proteobacteria may be attributed to loss of soluble fiber rather than the high proportion of dietary fat [37].”
BackgroundIntestinal Dysbiosis Contributes to the Delayed Gastrointestinal Transit in High-Fat Diet Fed Mice
Anitha, M., Reichardt, F., Tabatabavakili, S., Nezami, B. G., Chassaing, B., Mwangi, S. M., Vijay–Kumar, M., Gewirtz, A. T., & Srinivasan, S. (2016) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2015.12.008 · Cited by 139
“In a study comparing patients with irritable bowel syndrome with healthy controls, an increase in the Firmicutes to Bacteroidetes ratio was observed,(17,18) potentially contributing to symptoms such as constipation in irritable bowel syndrome patients.(19,20) Gut microbial products signal through the pathogen recognit…”
BackgroundThe mind-body-microbial continuum
Gonzalez, A., Stombaugh, J., Lozupone, C., Turnbaugh, P. J., Gordon, J. I., & Knight, R. D. (2011) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2011.13.1/agonzalez · Cited by 134
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“Multiple studies have shown that bacterial composition shifts to either gram positive majority or gram negative majority based on the composition of the diet consumed [30,36,37].”
Background
Metadata
- Authors
- Hildebrandt, M. A., Hoffmann, C., Sherrill–Mix, S. A., Keilbaugh, S. A., Hamady, M., Chen, Y., Knight, R., Ahima, R. S., Bushman, F., & Wu, G. D.
- Affiliations
- University of Pennsylvania (US)
- University of Colorado Boulder (US)
- Corresponding author
- Bushman, Frederic
- Wu, Gary D.
- Venue
- Gastroenterology
- Publisher
- Elsevier BV
- Published
- 2009-11
- Volume
- 137
- Issue
- 5
- Pages
- 1716-1724.e2
- ISSN
- 0016-5085 (ISSN-L)
- PMC
- PMC2770164
- OpenAlex
- W2158630697
- Cited by
- 1,576
- References
- 43
- Citations by year
- 2026: 40 · 2025: 61 · 2024: 96 · 2023: 76 · 2022: 130 · 2021: 117 · 2020: 158 · 2019: 148 · 2018: 115 · 2017: 94 · 2016: 104 · 2015: 96 · 2014: 87 · 2013: 82 · 2012: 71
- FWCI
- 22.84
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Gastroenterology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- University of Pennsylvania
- National Institutes of Health
- National Human Genome Research Institute (R01HG004872, HG004872)
- National Institute of General Medical Sciences (T32GM065103)
- National Institute of Allergy and Infectious Diseases (R01AI039368, AI39368)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK-50306, DK078669, P01DK078669, DK-019525, DK062348, R01DK062348, R56DK062348, P30DK019525, P30DK050306)
- National Center for Research Resources (S10RR024525)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Keywords
- gut microbiota, high-fat diet, obesity, diet-induced obesity, Bacteroidetes, Firmicutes, Proteobacteria, gut microbiota composition, metagenomics, microbial gene content, 16S rRNA gene sequencing
- MeSH terms
- Animals, Diet, Dietary Fats, Female, Hormones, Ectopic, Intestines, Mice, Inbred C57BL, Obesity, RNA, Ribosomal, 16S, Mice, Knockout, Intercellular Signaling Peptides and Proteins, Mice, Metagenome
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