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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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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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Patterns of the fecal microbiota in the Juan Fernández fur seal (Arctocephalus philippii)
Toro‐Valdivieso, C., Toro, F., Stubbs, S. C. B., Castro‐Nallar, E., & Blacklaws, B. (2021) · MicrobiologyOpen · doi:10.1002/mbo3.1215 · Cited by 18
“(b) Relative abundance per sample grouped by location: EA = El Arenal, BP = Bahia El Padre, PC = Piedra Carvajal, PT = Punta Truenos, SC = Santa Clara, TB = Tierras Blancas, V = Vaqueria EA BP P.C P.T SC TB V 18 JF FS 13 18 JF FS 81 2 17 JF FS 26 18 JF FS 14 18 JF FS 10 18 JF FS 9 18 JF FS 12 18 JF FS 11 17 JF FS 15 1…”
BackgroundInfluential‘Omics’‐driven discoveries in prevention and treatment of type 2 diabetes
Gjesing, A. P., & Pedersen, O. B. (2012) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.2012.02678.x · Cited by 18
The hybrid science of diet, microbes, and metabolic health
Shanahan, F., & Murphy, E. (2011) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.018473 · Cited by 18
Han, G., Lee, J.-Y., Jin, G.-D., Park, J., Choi, Y. H., Chae, B. J., Kim, E. B., & Choi, Y. (2016) · Veterinary Microbiology · doi:10.1016/j.vetmic.2016.10.020 · Cited by 18
RetractedImmunometabolism in type 2 diabetes mellitus: tissue-specific interactions
Pinheiro-Machado, E., Gurgul-Convey, E., & Marzec, M. (2020) · Archives of Medical Science · doi:10.5114/aoms.2020.92674 · Cited by 19
“High fat or high sugar diets were shown to induce imbalance in the ratio of specific strains of bacteria within the gut microbiota (Firmicutes/Bacteroidetes) and increase amounts of pro-inflammatory strains such as Proteobacteria [149, 150].”
BackgroundZhang, L., Lan, Y., Wang, Y., Yang, Y., Han, W., Li, J., Wang, Y., & Liu, X. (2022) · Food & Function · doi:10.1039/d1fo04037e · Cited by 17
Reemst, K., Tims, S., Yam, K., Mischke, M., Knol, J., Brul, S., Schipper, L., & Kőrösi, A. (2022) · mSystems · doi:10.1128/msystems.00180-22 · Cited by 19
Carlo, P. D., Serra, N., Alduina, R., Guarino, R., Craxı̀, A., Giammanco, A., Fasciana, T., Cascio, A., & Sergi, C. M. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.888233 · Cited by 18
“On this issue, metatranscriptomic studies conducted on laboratory animals such as mice or human fecal samples have recently shown that the harmful action of secondary BAs derives from primary BAs in the genesis of intestinal inflammatory processes and pancreatic cancer (Hildebrandt et al., 2009; Islam et al., 2011; Ma…”
BackgroundMale infertility risk and gut microbiota: a Mendelian randomization study
Fu, Z.-D., Wang, Y., & Yan, H. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1228693 · Cited by 18
“A high-fat diet (HFD) induces disruption of the gut microbiome, as reflected by decreases in Bacteroides and increases in Firmicutes and Aspergillus in mice models (Hildebrandt et al., 2009; Graham et al., 2015).”
BackgroundPostprandial Dysmetabolism and Its Medical Implications
Sasso, E., Batičić, L., & Tokmadžić, V. S. (2023) · Life · doi:10.3390/life13122317 · Cited by 19
“…, Streptococcus and Desulfovibrionaceae . obesity, and a high ratio of Firmicutes to Bacteroidetes has been found in obese humans [23,24] These data have Another critical factor that triggers inflammation is the imbalance of energy in adipocytes Recent scientific studies have…”
BackgroundManoharan, D., Sivakumar, N., Billamboz, M., & Jawhara, S. (2024) · Applied Microbiology · doi:10.3390/applmicrobiol4010017 · Cited by 18
Immunity-Based Evolutionary Interpretation of Diet-Induced Thermogenesis
Liao, W.-H., Henneberg, M., & Langhans, W. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.05.002 · Cited by 18
Mandalari, G., Chessa, S., Bisignano, C., Chan, L. S., & Carughi, A. (2016) · Food & Function · doi:10.1039/c6fo01137c · Cited by 19
Okubo, H., Kushiyama, A., Nakatsu, Y., Yamamotoya, T., Matsunaga, Y., Fujishiro, M., Sakoda, H., Ohno, H., Yoneda, M., & Asano, T. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19103064 · Cited by 18
A comparative study of gut microbiomes in captive nocturnal strepsirrhines
Bornbusch, S. L., Greene, L. K., McKenney, E. A., Volkoff, S. J., Midani, F. S., Joseph, G., Gerhard, W. A., Iloghalu, U. B., Granek, J. A., & Gunsch, C. K. (2019) · American Journal of Primatology · doi:10.1002/ajp.22986 · Cited by 19
“…GMBs were enriched for bacteria from seven phyla, including taxa associated with a range of dietary substrates such as fat (Desulfovibrionaceae; Hildebrandt et al., 2009), fiber (Ruminococcaceae; Daly et al., 2012), and starch (Parabacteroides; Martínez, Kim, Duffy, Schlegel, & Walter, 2010;…”
BackgroundDietary Management of Pediatric Inflammatory Bowel Disease
Kaenkumchorn, T. K., & Kesavan, A. (2019) · Journal of Medicinal Food · doi:10.1089/jmf.2019.0063 · Cited by 17
Moreno‐Indias, I., Lundberg, R., Krych, Ł., Metzdorff, S. B., Kot, W., Sørensen, D. B., Nielsen, D. S., Hansen, C. H. F., & Hansen, A. K. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01336 · Cited by 18
Hua, Y., Cao, H., Wang, J., He, F., & Jiang, G. (2020) · BMC Veterinary Research · doi:10.1186/s12917-020-02583-1 · Cited by 17
Morbidly obese subjects show increased serum sulfide in proportion to fat mass
Comas, F., Latorre, J., Ortega, F. J., Arnoriaga‐Rodríguez, M., Lluch, A., Sabater, M., Rius, F., Ribas, X., Costas, M., Ricart, W., et al. (2020) · International Journal of Obesity · doi:10.1038/s41366-020-00696-z · Cited by 17
“Of note, metagenomic studies pointed to increased sulfate-reducing bacteria in obesogenic conditions [47, 48].”
BackgroundLa microbiota intestinal: Un nuevo actor en el desarrollo de la obesidad
Morales, P., Brignardello, J., & Gotteland, M. (2010) · Revista médica de Chile · doi:10.4067/s0034-98872010000800013 · Cited by 17
Plasma levels of resistin-like molecule beta in humans
Neilson, A. P., Djurić, Z., Land, S. J., & Kato, I. (2010) · Cancer Epidemiology · doi:10.1016/j.canep.2010.10.007 · Cited by 17
“RELMb expression is induced by intestinal microbial colonization, and RELMb plays a key role in epithelial barrier function and integrity [5–8].”
Backgroundda Silva, A. V. A., Oliveira, S. B., Rienzi, S. C. D., Brown-Steinke, K., Dehan, L. M., Rood, J. K., Carreira, V., Le, H., Maier, E. A., Betz, K., et al. (2018) · Current Developments in Nutrition · doi:10.1093/cdn/nzy070 · Cited by 16
“Others have described microbiome shifts (specifically a decrease in Bacteriodetes and an expansion of Proteobacteria and Firmicutes) inmice subjected to a high-fat diet (39).”
BackgroundTafti, Z. S. M., Moshiri, A., Marvasti, F. E., Tarashi, S., Khalili, S. F. S., Motahhary, A., Fateh, A., Vaziri, F., Badi, S. A., & Siadat, S. D. (2019) · Gastroenterology and hepatology from bed to bench. · Cited by 17
Li, W., Ma, T., Zhang, N., Deng, K., & Diao, Q. (2023) · Journal of Integrative Agriculture · doi:10.1016/j.jia.2023.06.037 · Cited by 18
Alleviation of colonic inflammation by Lypd8 in a mouse model of inflammatory bowel disease
Hsu, C.-C., Okumura, R., Motooka, D., Sasaki, R., Nakamura, S., Iida, T., & Takeda, K. (2021) · International Immunology · doi:10.1093/intimm/dxab012 · Cited by 15
Millar, C. L., Anto, L., Garcia, C., Kim, M., Jain, A., Provatas, A. A., Clark, R. B., Lee, J., Nichols, F. C., & Blesso, C. N. (2022) · Journal of Lipid Research · doi:10.1016/j.jlr.2022.100192 · Cited by 16
Que, T., Pang, X., Huang, H., Chen, P., Wei, Y., Hua, Y., Liao, H., Wu, J., Li, S., Wu, A., et al. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.872841 · Cited by 16
Eating away cancer: the potential of diet and the microbiome for shaping immunotherapy outcome
Nguyen, N.-T. A., Jiang, Y., & McQuade, J. L. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1409414 · Cited by 19
Lu, X., Jing, Y., Zhang, N., Chen, L., Tai, J., & Cao, Y. (2024) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2024.122870 · Cited by 17
Kalmokoff, M. L., Franklin, J., Petronella, N., Green, J., & Brooks, S. P. J. (2015) · Nutrients · doi:10.3390/nu7053279 · Cited by 16
“Finally, it is of interest to note that a commonly observed change in the gut community of obese rodents fed high energy diets has been a shift in the gut community towards the phylum Firmicutes [4,19], and various explanations have been forwarded to explain this observation [73,74].”
BackgroundIntrinsic association between diet and the gut microbiome: current evidence
Fodor, A. A., & Winglee, K. (2015) · Nutrition and Dietary Supplements · doi:10.2147/nds.s62362 · Cited by 16
Lymphotoxin organizes contributions to host defense and metabolic illness from innate lymphoid cells
Upadhyay, V., & Fu, Y. (2013) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2013.12.007 · Cited by 16
“It is intriguing to note that mice lacking RELMb resist weight gain and have altered microbiota [91], however whether the LT-pathway regulates RELMb is unappreciated.”
BackgroundGraf, B. L., Zhang, L., Corradini, M. G., Kuhn, P. E., Newman, S. S., Salbaum, J. M., & Raskin, I. (2018) · Journal of Functional Foods · doi:10.1016/j.jff.2018.04.032 · Cited by 19
Bayesian Graphical Compositional Regression for Microbiome Data
Mao, J., Chen, Y., & Ma, L. (2019) · Journal of the American Statistical Association · doi:10.1080/01621459.2019.1647212 · Cited by 16
“(Hildebrandt et al. 2009; Wu et al. 2011; Qin et al. 2012; David et al. 2014).”
BackgroundSelf-citationPlissonneau, C., Sivignon, A., Chassaing, B., Capel, F., Martin, V., Etienne, M., Wawrzyniak, I., Chaussé, P., Dutheil, F., Mairesse, G., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23115891 · Cited by 21
Dietary and Flight Energetic Adaptations in a Salivary Gland Transcriptome of an Insectivorous Bat
Phillips, C. J., Phillips, C. D., Goecks, J., Lessa, E. P., de Sotero-Caio, C. G., Tandler, B., Gannon, M. R., & Baker, R. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0083512 · Cited by 18
“Its normal secretion is triggered by lipids in the intestine and in fact RETNLB gene expression is up-regulated by a high fat diet [27].”
BackgroundMasarwi, M., Solnik-Isaac, H., Phillip, M., Yaron, S., Shamir, R., Pasmanic-Chor, M., & Gat‐Yablonski, G. (2017) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2017.08.014 · Cited by 16
Guo, Z., Hu, B., Wang, H., Kong, L., Han, H., Li, K., Sun, S., Lei, Z., Shimizu, K., & Zhang, Z. (2020) · Journal of Functional Foods · doi:10.1016/j.jff.2020.103820 · Cited by 16
“…HFD feeding could induce a large alteration in the composition of gut microbiota in mice, which is characterized by a huge increase in the relative abundance of phylum Firmicutes and a sharp decrease in the relative abundance of phylum Bacteroidetes (Hildebrandt et al., 2009; Liu et al., 2018).”
InfluentialHigh-Fat Diets Led to OTU-Level Shifts in Fecal Samples of Healthy Adult Dogs
Kilburn, L., Koester, L. R., Schmitz‐Esser, S., Serão, N. V. L., & Serao, M. C. R. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.564160 · Cited by 17
“Coelho et al. (2018) reported an increase in the Firmicutes:Bacteroides ratio with the switch to a diet with increased protein levels and reduced carbohydrate levels.”
BackgroundInfluential
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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