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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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ResultThe gut microbiome in cardio-metabolic health
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“Retnlb 16 Fifteen Bacteriodetes lineages, and 1 lineage of Proteobacteria, changed in abundance between genotypes, whereas 15 Firmicutes lineages changed in abundance (Hildebrandt et al. 2009)”
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BackgroundDietary nutrition and gut microflora: A promising target for treating diseases
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BackgroundDietary Fatty Acids Sustain the Growth of the Human Gut Microbiota
Agans, R., Gordon, A., Kramer, D. L., Pérez-Burillo, S., Rufián‐Henares, J. Á., & Paliy, O. (2018) · Applied and Environmental Microbiology · doi:10.1128/aem.01525-18 · Cited by 108
“This conclusion is supported by multiple studies which showed that a high-fat diet leads to significant alterations in gut microbial communities in both humans and animals (15, 16).”
BackgroundResultJang, H. R., Park, H., Kang, D., Chung, H., Nam, M. H., Lee, Y., Park, J., & Lee, H. (2019) · Experimental & Molecular Medicine · doi:10.1038/s12276-019-0293-4 · Cited by 105
Tokuhara, D. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.700058 · Cited by 106
A Western Diet Increases Serotonin Availability in Rat Small Intestine
Bertrand, R. L., Senadheera, S. N., Markus, I., Liu, L., Howitt, L., Chen, H., Murphy, T. V., Sandow, S. L., & Bertrand, P. P. (2010) · Endocrinology · doi:10.1210/en.2010-0377 · Cited by 100
“intestinal microflora (56, 57), which in turn has been”
BackgroundEberl, C., Ring, D., Münch, P. C., Beutler, M., Basic, M., Slack, E. M. C., Schwarzer, M., Šrůtková, D., Lange, A., Frick, J.-S., et al. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.02999 · Cited by 98
Obesity, Metabolic Syndrome, and Microbiota
Tilg, H. (2010) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e3181dd8b64 · Cited by 103
“Hildebrandt et al recently presented data on how a high-fat diet might affect the composition of the murine gut microbiome, even independent of obesity.(22) In this study, the investigators compared wild-type and RELMb-deficient mice and assessed the influence of diet, genotype, and obesity on the microbiome compositi…”
BackgroundKisuse, J., La-ongkham, O., Nakphaichit, M., Therdtatha, P., Momoda, R., Tanaka, M., Fukuda, S., Popluechai, S., Kespechara, K., Sonomoto, K., et al. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01345 · Cited by 101
“The F/B ratio is known to be positively correlated with high-fat dietinduced obesity (Ley et al., 2006; Turnbaugh et al., 2008, 2009; Hildebrandt et al., 2009; Zhang et al., 2012).”
BackgroundFecal dysbiosis in infants with cystic fibrosis is associated with early linear growth failure
Hayden, H. S., Eng, A., Pope, C. E., Brittnacher, M., Vo, A. T., Weiss, E. J., Hager, K. R., Martin, B. D., Leung, D. H., Heltshe, S. L., et al. (2020) · Nature Medicine · doi:10.1038/s41591-019-0714-x · Cited by 97
Shi, L., Li, Y., Wang, Y., & Feng, Y. (2015) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2015.08.057 · Cited by 101
Shifts in the Midgut/Pyloric Microbiota Composition within a Honey Bee Apiary throughout a Season
Ludvigsen, J., Rangberg, A., Avershina, E., Sekelja, M., Kreibich, C. D., Amdam, G. V., & Rudi, K. (2015) · Microbes and Environments · doi:10.1264/jsme2.me15019 · Cited by 99
“We favored environmental exposure and dietary changes as the main drivers for seasonal trends because of the strong relationship that exists between gut bacterial composition and the host diet in humans, vertebrate animals, and insects (7, 12, 14, 24).”
Backgroundde Souza, A. Z. Z., Zambom, A. Z., Abboud, K. Y., Reis, S. K., Tannihão, F., Guadagnini, D., Saad, M. J. A., & Prada, P. O. (2015) · Nutrition · doi:10.1016/j.nut.2015.01.004 · Cited by 99
“Similar results were observed in human [17,18] and animal [16,19–21] studies.”
ResultKelly, C. J., Colgan, S. P., & Frank, D. N. (2012) · Nutrition in Clinical Practice · doi:10.1177/0884533611434934 · Cited by 103
Gut Microbiota and Lifestyle Interventions in NAFLD
Houghton, D., Stewart, C. J., Day, C. P., & Trenell, M. I. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17040447 · Cited by 99
“Changes in gut microbiota are also associated with appetite regulation, improved glucose tolerance, increased satiety, reduced ghrelin, plasma triglycerides, oxidative stress and inflammation and calories consumed [82,158–160].”
BackgroundHan, G., Lee, J.-Y., Jin, G.-D., Park, J., Choi, Y. H., Chae, B. J., Kim, E. B., & Choi, Y. (2017) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-017-8304-7 · Cited by 99
“…ratio compared with that of the lighter group, whereas a significantly higher Bacteroidetes level was observed in the microbiota of the lighter group, consistent with the results observed in many previous studies (Delzenne and Cani 2011; Hildebrandt et al. 2009; Ley et al. 2006; Kasai et al. 2015).”
Dunn, C. M., Velasco, C., Rivas, A., Andrews, M., Sturdy, C., Jacob, P. B., & Jeffries, M. A. (2020) · Arthritis & Rheumatology · doi:10.1002/art.41210 · Cited by 96
“Proteobacteria have been observed in mice fed a highfat diet (49).”
BackgroundTan, R., Dong, H., Chen, Z., Jin, M., Yin, J., Li, H., Shi, D., Shao, Y., Wang, H., Chen, T., et al. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.654074 · Cited by 100
“In mice, regardless of the genotype studied, the intake of a high-fat diet (HFD) or high-fat high-sugar western diet (HFHSD) was associated with decreased Bacteroides levels and increased Firmicutes and Proteobacteria, in a dose-dependent manner (Hildebrandt et al., 2009).”
BackgroundObesity and the gut microbiome: Striving for causality
Harley, I. T. W., & Karp, C. L. (2012) · Molecular Metabolism · doi:10.1016/j.molmet.2012.07.002 · Cited by 99
Anhê, F. F., Varin, T. V., Barz, M. L., Pilon, G., Dudonné, S., Trottier, J., St‐Pierre, P., Harris, C. S., Lucas, M., Lemire, M., et al. (2017) · Diabetologia · doi:10.1007/s00125-017-4520-z · Cited by 104
“As previously reported [14, 25], functions related to cell motility (i.”
BackgroundZhou, L., Xiao, X., Zhang, Q., Zheng, J., Li, M., Yu, M., Wang, X., Deng, M., Zhai, X., & Li, R. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00516 · Cited by 96
“The phylum Proteobacteria, class Deltaproteobacteria, order Desulfovibrionales, family Frontiers in Endocrinology | www.frontiersin.org 5 September 2018 | Volume 9 | Article 516 FIGURE 4 | PCA plots of gut communities in the female offspring at weaning (n = 6–8/group).”
BackgroundInfluentialIs there any association between gut microbiota and type 1 diabetes? A systematic review
Jamshidi, P. K., Hasanzadeh, S., Tahvildari, A., Farsi, Y., Arbabi, M., Mota, J. F., Sechi, L. A., & Nasiri, M. J. (2019) · Gut Pathogens · doi:10.1186/s13099-019-0332-7 · Cited by 104
Khan, M. S., Ikram, M. A., Park, J. S., Park, T. J., & Kim, M. O. (2020) · Cells · doi:10.3390/cells9040853 · Cited by 99
Diet Alters Entero-Mammary Signaling to Regulate the Breast Microbiome and Tumorigenesis
Soto‐Pantoja, D. R., Gaber, M. K., Arnone, A. A., Bronson, S. M., Cruz‐Diaz, N., Wilson, A. S., Clear, K. Y. J., Ramirez, M. U., Kucera, G. L., Levine, E. A., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-20-2983 · Cited by 97
Modelling the role of microbial p-cresol in colorectal genotoxicity
Hinai, E. A., Kullamethee, P., Rowland, I. R., Swann, J. R., Walton, G., & Commane, D. M. (2018) · Gut Microbes · doi:10.1080/19490976.2018.1534514 · Cited by 96
Molina‐Tijeras, J. A., Diez‐Echave, P., Vezza, T., Hidalgo‐Garcia, L., Ruiz‐Malagón, A. J., Rodríguez‐Sojo, M. J., Romero, M., Robles‐Vera, I., García, F., Plaza‐Díaz, J., et al. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105471 · Cited by 100
Temporal stability of the mouse gut microbiota in relation to innate and adaptive immunity
Dimitriu, P. A., Boyce, G. K., Samarakoon, A., Hartmann, M., Johnson, P., & Mohn, W. W. (2012) · Environmental Microbiology Reports · doi:10.1111/j.1758-2229.2012.00393.x · Cited by 95
Wankhade, U. D., Zhong, Y., Kang, P., Alfaro, M., Chintapalli, S. V., Piccolo, B. D., Mercer, K. E., Andres, A., Thakali, K. M., & Shankar, K. (2018) · Scientific Reports · doi:10.1038/s41598-018-34453-0 · Cited by 100
Intestinal Microbiota Modulation in Obesity-Related Non-alcoholic Fatty Liver Disease
Porras, D., Nistal, E., Martínez‐Flórez, S., González‐Gallego, J., García‐Mediavilla, M. V., & Sánchez‐Campos, S. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01813 · Cited by 97
“In nutritional models of obesity in mice using high fat diets (HFD), increased Firmicutes/Bacteroidetes ratio is a common outcome (Turnbaugh et al., 2008; Hildebrandt et al., 2009; Murphy et al., 2010) but it was suggested that this may be a feature of the diet rather than an obesity marker (Marchesi et al.”
BackgroundRelationship between the microbiome and ocular health
Cavuoto, K. M., Banerjee, S., & Galor, A. (2019) · The Ocular Surface · doi:10.1016/j.jtos.2019.05.006 · Cited by 95
Management of metabolic syndrome through probiotic and prebiotic interventions
Grover, S., Mallappa, R., Rokana, N., Duary, R. K., Panwar, H., & Batish, V. K. (2011) · Indian Journal of Endocrinology and Metabolism · doi:10.4103/2230-8210.91178 · Cited by 101
Parekh, P. J., Arusi, E., Vinik, A. I., & Johnson, D. A. (2014) · Frontiers in Endocrinology · doi:10.3389/fendo.2014.00047 · Cited by 99
Long-term activation of the innate immune system in atherosclerosis
Christ, A., Bekkering, S., Latz, E., & Riksen, N. P. (2016) · Seminars in Immunology · doi:10.1016/j.smim.2016.04.004 · Cited by 96
Alteration of gut microbiota induced by DPP-4i treatment improves glucose homeostasis
Liao, X., Song, L., Zeng, B., Liu, B., Qiu, Y., Qu, H., Zheng, Y., Long, M., Zhou, H., Wang, Y., et al. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2019.03.057 · Cited by 98
“Previous studies have revealed that HFD results in a shift of the gutmicrobiota that is correlated with increasing plasma glucose and glucose intolerance [17,56,57].”
BackgroundWang, S., Li, Q., Zang, Y., Zhao, Y., Liu, N., Wang, Y., Xu, X., Liu, L., & Mei, Q. (2017) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2017.02.074 · Cited by 97
Toll-like receptors and metabolic (dysfunction)-associated fatty liver disease
Khanmohammadi, S., & Kuchay, M. S. (2022) · Pharmacological Research · doi:10.1016/j.phrs.2022.106507 · Cited by 95
Liu, T., Hougen, H. Y., Vollmer, A. C., & Hiebert, S. M. (2012) · Anaerobe · doi:10.1016/j.anaerobe.2012.02.004 · Cited by 100
“Given that Actinobacteria levels have been found to be elevated in obese individuals [48] and in mice on a high-fat diet [9], further investigations could reveal whether Actinobacteria levels are influenced by type of dietary fat.”
BackgroundResultInfluentialPrieto, I., Hidalgo, M., Segarra, A. B., Martínez-Rodríguez, A. M., Cobo, A., Ramírez, M., Abriouel, H., Gálvez, A., & Martínez-Cañamero, M. (2018) · PLoS ONE · doi:10.1371/journal.pone.0190368 · Cited by 91
Gut Microbiome Signatures Are Biomarkers for Cognitive Impairment in Patients With Ischemic Stroke
Ling, Y., Gong, T., Zhang, J., Gu, Q., Gao, X., Weng, X., Liu, J., & Sun, J. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.511562 · Cited by 92
Ondee, T., Pongpirul, K., Visitchanakun, P., Saisorn, W., Kanacharoen, S., Wongsaroj, L., Kullapanich, C., Ngamwongsatit, N., Settachaimongkon, S., Somboonna, N., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-85449-2 · Cited by 90
Yoon, S. J., Yu, J. S., Min, B. H., Gupta, H., Won, S., Park, H., Han, S. H., Kim, B., Kim, K. H., Kim, B. K., et al. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1129904 · Cited by 92
“While the mechanisms are still poorly understood, our results are in agreement with a previous study that reported the same trends in mice fed a high-fat diet (Hildebrandt et al., 2009).”
ResultGenes and Environment: How Will Our Concepts on the Pathophysiology of IBD Develop in the Future?
Kaser, A., Zeißig, S., & Blumberg, R. S. (2010) · Digestive Diseases · doi:10.1159/000320393 · Cited by 97
Patterns and Processes in Parasite Co-Infection
Viney, M., & Graham, A. L. (2013) · Advances in Parasitology/Advances in parasitology · doi:10.1016/b978-0-12-407706-5.00005-8 · Cited by 95
Dietary fat and gut microbiota: mechanisms involved in obesity control
Coelho, O. G. L., Cândido, F. G., & Alfenas, R. D. C. G. (2018) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2018.1481821 · Cited by 90
Busnelli, M., Manzini, S., & Chiesa, G. (2019) · Nutrients · doi:10.3390/nu12010079 · Cited by 92
Qiu, X., Macchietto, M. G., Liu, X., Lu, Y., Ma, Y., Guo, H., Saqui–Salces, M., Bernlohr, D., Chen, C., Shen, S., et al. (2020) · International Journal of Obesity · doi:10.1038/s41366-020-00712-2 · Cited by 90
“Gut microbiota composition is reshaped in obese individuals [7, 26, 27, 39], which is characterized by dysbiosis, a decrease in microbiota diversity.”
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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