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The Effect of Diet on the Human Gut Microbiome: A Metagenomic Analysis in Humanized Gnotobiotic Mice
Open accessAbstract
A translational medicine pipeline is described where human gut microbial communities and diets are re-created in gnotobiotic mice and the impact on microbe and host is defined using metagenomics.
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“The majority of studies in humans and mice rely on faecal samples, which provide some representation of what is occurring throughout the digestive tract”
From Diet–microbiota interactions as moderators of human metabolism (2016) · cites this paper as [120]
In the citing paper
“aspects of microbial communities and host responses that are specific to the small intestine might be obscured by faecal sampling119,120.”
From Diet–microbiota interactions as moderators of human metabolism (2016) · cites this paper as [120]
In the citing paper
“Our study corroborates previous studies showing an association between altered diets and an increase in Erysipelotrichi and Allobaculum, but various effects are shown for fat-enriched diets 29, 30, 31, 32.”
From The composition of the gut microbiota shapes the colon mucus barrier (2015) · cites this paper as [32]
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 [206]
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InfluentialBeneficial Effect of Intestinal Fermentation of Natural Polysaccharides
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“In the future, investigation of shared microbial functional outcomes between animals and humans and utilization of humanized animals inoculated with human gut microbiota may help obtain clinically relevant data for the translation of basic discovery to humans (195, 196).”
BackgroundNew Insights Into the Cancer–Microbiome–Immune Axis: Decrypting a Decade of Discoveries
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Discovering new indicators of fecal pollution
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The epithelial barrier theory and its associated diseases
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Parental Dietary Fat Intake Alters Offspring Microbiome and Immunity
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“Human gut microbiomes are more dynamic than mice raised in controlled, specific pathogen-free cages (36).”
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BackgroundViral communities of the human gut: metagenomic analysis of composition and dynamics
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“Gut bacteria are affected by diet [71, 72], so diet is”
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“Sample sizes were chosen on the basis of similar prior studies (12, 22, 50) and logistical constraints within gnotobiotic isolators.”
BackgroundMethodInfluentialBisphenol A alters gut microbiome: Comparative metagenomics analysis
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BackgroundDirected Culturing of Microorganisms Using Metatranscriptomics
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The Gut Microbiome in Hypertension
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The "Gut Feeling": Breaking Down the Role of Gut Microbiome in Multiple Sclerosis
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Gut microbiota and metabolic disorders: how prebiotic can work?
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“Interestingly, the transfer of this modi-fied gut microbiota to germ-free mice also transfers the obese phenotype (13) .”
Stereotypes About Enterotype: The Old and New Ideas
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Gut Microbiota: From Microorganisms to Metabolic Organ Influencing Obesity
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“(95) colonized mice with human feces and fed them a Western diet versus a low-fat diet rich in plant polysaccharides for 2 weeks, then transplanted their microbiota to germ-free mice.”
BackgroundCo-evolution in context: The importance of studying gut microbiomes in wild animals
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“…have been linked to the development of a number of pathological states (such as obesity, allergy, diabetes, Crohn’s disease, irritable colon syndrome, and cancer) are known to drive microbiome alterations and lead to dysbiosis (Turnbaugh et al., 2009; Leclercq et al., 2014; Allais et al., 2016).”
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Metagenomic Approaches for Understanding New Concepts in Microbial Science
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Gut microbiome-Mediterranean diet interactions in improving host health
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“As mentioned above, diet shapes the gut microbiome by supplying specific substrates that differentially foster the growth of specific gut microbial communities 87–89 ; this diet-microbiome network is universally consistent in human and animal studies 85,87,90,91 .”
BackgroundCultivating Healthy Growth and Nutrition through the Gut Microbiota
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Self-citationGut microbiota, the pharmabiotics they produce and host health
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“Metagenomic studies go beyond the 16S rRNA gene to sequence small fragments of metagenomic DNA at random to characterise the full genetic content and functional potential of the microbial community((2,24,25)).”
BackgroundThe gut microbiome in autoimmunity: Sex matters
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BackgroundImpact of Westernized Diet on Gut Microbiota in Children on Leyte Island
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“found that switching mice from a low-fat, plant-rich diet to a high-fat, high-sugar diet could change microbial composition and metabolism in as little as a day (93), and the same group demonstrated alterations to the human gut microbiota after only 4 days on a plant-based or animal-based diet (94).”
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BackgroundThe gut microbiota in mouse models of inflammatory bowel disease
Gkouskou, K. K., Deligianni, C., Tsatsanis, C., & Eliopoulos, A. G. (2014) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2014.00028 · Cited by 164
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The Impact of Gut Microbiota Disorders on the Blood–Brain Barrier
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Gut microbiota composition correlates with changes in body fat content due to weight loss
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“Mice colonized with human feces establish a complex microbiota [12].”
BackgroundIntegrating nutrition and immunology: A new frontier
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BackgroundPrebiotics: Definition and protective mechanisms
Valcheva, R. S., & Dieleman, L. A. (2016) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2016.02.008 · Cited by 177
Effects of a high fat diet on intestinal microbiota and gastrointestinal diseases
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A Guide to Diet-Microbiome Study Design
Johnson, A. J., Zheng, J. J., Kang, J. W., Saboe, A., Knights, D., & Zivkovic, A. M. (2020) · Frontiers in Nutrition · doi:10.3389/fnut.2020.00079 · Cited by 168
Duca, F. A., Sakar, Y., Lepage, P., Devime, F., Goustard, B., Dore, J. M., & Covașă, M. (2014) · Diabetes · doi:10.2337/db13-1526 · Cited by 169
“Interestingly, HF feeding causes rapid microbiota shifts occurring before changes in adiposity (29), suggesting that direct microbe host cross talk influences intestinal-signaling mechanisms that precede and result in hyperphagia and promote weight gain.”
BackgroundInfluentialRetractedNew insights into the mechanisms of high‐fat diet mediated gut microbiota in chronic diseases
Chen, J., Xiao, Y., Li, D., Zhang, S., Wu, Y., Zhang, Q., & Bai, W. (2023) · iMeta · doi:10.1002/imt2.69 · Cited by 178
“Turnbaugh et al. [63] revealed that after consuming HF/HSD, a higher proportion of the members of the Erysipelotrichi and Bacilli classes of the Firmicutes was observed compared with the control group.”
ResultChiu, C.-C., Ching, Y.-H., Li, Y.-P., Liu, J.-Y., Huang, Y.-T., Huang, Y.-W., Yang, S.-S., Huang, W.-C., & Chuang, H.-L. (2017) · Nutrients · doi:10.3390/nu9111220 · Cited by 160
“The level of Bacteroidetes is significantly lower in obese subjects as compared with normal-weight subjects [13].”
BackgroundNext-generation and whole-genome sequencing in the diagnostic clinical microbiology laboratory
Dunne, W. M., Westblade, L. F., & Ford, B. A. (2012) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-012-1641-7 · Cited by 161
Shen, W., Gaskins, H. R., & McIntosh, M. (2013) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2013.09.009 · Cited by 166
“[56] demonstrated using a humanized mouse model”
Saresella, M., Mendozzi, L., Rossi, V., Mazzali, F., Piancone, F., LaRosa, F., Marventano, I., Caputo, D., Felis, G. E., & Clerici, M. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01391 · Cited by 162
Gut Microbiome Composition in Non-human Primates Consuming a Western or Mediterranean Diet
Nagpal, R., Shively, C. A., Appt, S. A., Register, T. C., Michalson, K. T., Vitolins, M. Z., & Yadav, H. (2018) · Frontiers in Nutrition · doi:10.3389/fnut.2018.00028 · Cited by 163
“Diet-microbiome interactions are consistently reproducible in clinical and animal studies [5, 8, 10, 11].”
BackgroundGuo, X., Li, J., Tang, R., Zhang, G., Zeng, H., Wood, R. J., & Liu, Z. (2017) · Mediators of Inflammation · doi:10.1155/2017/9474896 · Cited by 171
Gutted! Unraveling the Role of the Microbiome in Major Depressive Disorder
Bastiaanssen, T. F. S., Cussotto, S., Claesson, M. J., Clarke, G., Dinan, T. G., & Cryan, J. F. (2020) · Harvard Review of Psychiatry · doi:10.1097/hrp.0000000000000243 · Cited by 159
Bouret, S., Levin, B. E., & Ozanne, S. E. (2015) · Physiological Reviews · doi:10.1152/physrev.00007.2014 · Cited by 157
Montassier, E., Batard, É., Massart, S., Gastinne, T., Carton, T., Caillon, J., Fresne, S. L., Caroff, N., Hardouin, J.-B., Moreau, P., et al. (2014) · Microbial Ecology · doi:10.1007/s00248-013-0355-4 · Cited by 163
Murakami, M., Tognini, P., Liu, Y., Eckel‐Mahan, K. L., Baldi, P., & Sassone‐Corsi, P. (2016) · EMBO Reports · doi:10.15252/embr.201642463 · Cited by 161
“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).”
Irritable bowel syndrome: the role of food in pathogenesis and management.
Hayes, P. A., Fraher, M., & Quigley, E. M. M. (2014) · Europe PMC (PubMed Central) · Cited by 159
Community ecology as a framework for human microbiome research
Gilbert, J. A., & Lynch, S. V. (2019) · Nature Medicine · doi:10.1038/s41591-019-0464-9 · Cited by 163
Human-Associated Microbial Signatures: Examining Their Predictive Value
Knights, D., Parfrey, L. W., Zaneveld, J., Lozupone, C., & Knight, R. D. (2011) · Cell Host & Microbe · doi:10.1016/j.chom.2011.09.003 · Cited by 156
“For example, Turnbaugh et al. (2009) used a combination of genomic and transcriptomic approaches to study members of class Erysipelotrichi that increased when gnotobiotic mice, transplanted with a human microbial community, were switched from a low-fat diet rich in vegetables to a high-fat,…”
Self-citationMoody microbes or fecal phrenology: what do we know about the microbiota-gut-brain axis?
Forsythe, P., Kunze, W., & Bienenstock, J. (2016) · BMC Medicine · doi:10.1186/s12916-016-0604-8 · Cited by 162
“[118].”
Tinker, K. A., & Ottesen, E. A. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.01837-16 · Cited by 159
Mirzaei, M. K., Khan, M. A. A., Ghosh, P., Taranu, Z. E., Taguer, M., Ru, J., Chowdhury, R., Kabir, M. M., Deng, L., Mondal, D., et al. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.01.004 · Cited by 158
“The effects of these factors on gut bacterial communities have been reported numerous times, and their effect on phage communities might result from the changes in bacterial communities (HumanMicrobiome Project, 2012; Turnbaugh et al., 2009; Vonaesch et al., 2018).”
BackgroundFunctional attractors in microbial community assembly
Estrela, S., Vila, J. C. C., Lu, N., Bajić, D., Rebolleda‐Gómez, M., Chang, C., Goldford, J. E., Sánchez-Gorostiaga, A., & Sánchez, Á. (2021) · Cell Systems · doi:10.1016/j.cels.2021.09.011 · Cited by 153
The yin yang of bacterial polysaccharides: lessons learned from B. fragilis PSA
Surana, N. K., & Kasper, D. L. (2011) · Immunological Reviews · doi:10.1111/j.1600-065x.2011.01075.x · Cited by 160
“There is increasing evidence, however, that the exact composition of the human microbiota varies with diet, geography, and environmental exposures (18, 129, 130).”
BackgroundXiao, L., Sonne, S. B., Feng, Q., Chen, N., Xia, Z., Li, X., Fang, Z., Zhang, D., Fjære, E., Midtbø, L. K., et al. (2017) · Microbiome · doi:10.1186/s40168-017-0258-6 · Cited by 156
“Recent studies have further indicated that obesity is correlated with decreased microbial diversity or richness [11 – 13].”
BackgroundSocial networks strongly predict the gut microbiota of wild mice
Raulo, A., Allen, B. E., Troitsky, T. S., Husby, A., Firth, J. A., Coulson, T. N., & Knowles, S. C. L. (2021) · The ISME Journal · doi:10.1038/s41396-021-00949-3 · Cited by 152
Zhu, C., Sawrey-Kubicek, L., Beals, E., Rhodes, C. H., Houts, H. E., Sacchi, R., & Zivkovic, A. M. (2020) · Nutrition Research · doi:10.1016/j.nutres.2020.03.005 · Cited by 153
Epithelial barrier biology: good fences make good neighbours
Moens, E., & Veldhoen, M. (2011) · Immunology · doi:10.1111/j.1365-2567.2011.03506.x · Cited by 169
Jin, J., Touyama, M., Hisada, T., & Benno, Y. (2012) · Microbiology and Immunology · doi:10.1111/j.1348-0421.2012.00502.x · Cited by 157
“Despite intensive studies, it has been difficult to determine the characteristics and composition of the HIM because of inter-individual diversity and continuous alterations in the community, which is influenced by environmental exposure (8), diet (9, 10), drugs (e.”
BackgroundComparative evaluation of establishing a human gut microbial community within rodent models
Wos‐Oxley, M. L., Bleich, A., Oxley, A. P. A., Kahl, S., Janus, L. M., Smoczek, A., Nahrstedt, H., Pils, M. C., Taudien, S., Platzer, M., et al. (2012) · Gut Microbes · doi:10.4161/gmic.19934 · Cited by 160
“In contrast, the human-donor used in the experiments by Turnbaugh et al.(19) can be tentatively grouped into enterotype 2, mainly based on the high abundance of Prevotella spp.”
InfluentialThe Infant Gut Microbiome: Evidence for Obesity Risk and Dietary Intervention
Koleva, P. T., Bridgman, S. L., & Kozyrskyj, A. L. (2015) · Nutrients · doi:10.3390/nu7042237 · Cited by 158
“associated with higher proportions of the Firmicutes class, Erysipelotrichi, and lower abundance of Bacteroidetes phylum [12].”
BackgroundChallenges of metabolomics in human gut microbiota research
Smirnov, K. S., Maier, T. V., Walker, A., Heinzmann, S. S., Forcisi, S., Martínez, I., Walter, J., & Schmitt‐Kopplin, P. (2016) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2016.03.006 · Cited by 163
Chrono-Nutrition: Circadian Rhythm and Personalized Nutrition
Franzago, M., Alessandrelli, E., Notarangelo, S., Stuppia, L., & Vitacolonna, E. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032571 · Cited by 183
“On the other hand, a high-fat diet (HFD) affects the composition of the GM, leading to a drastic reduction in microbial diversity and the Firmicutes/Bacteroidetes ratio, as well as an increases in different bacteria from the Firmicutes phylum [123,124].”
BackgroundBiphasic assembly of the murine intestinal microbiota during early development
Pantoja-Feliciano, I. G., Clemente, J. C., Costello, E. K., Pérez, M.-E., Blaser, M. J., Knight, R. D., & Domínguez-Bello, M. G. (2013) · The ISME Journal · doi:10.1038/ismej.2013.15 · Cited by 152
“We confirmed that colon contents were good proxies for feces (Supplementary Figures S2–S5), as reported (Peterson et al., 2008; Turnbaugh et al., 2009).”
ResultSelf-citationRestructuring of the amphibian gut microbiota through metamorphosis
Kohl, K. D., Cary, T. L., Karasov, W. H., & Dearing, M. D. (2013) · Environmental Microbiology Reports · doi:10.1111/1758-2229.12092 · Cited by 149
Mechanisms of weight loss and improved metabolism following bariatric surgery
Mulla, C. M., Middelbeek, R. J. W., & Patti, M. (2017) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13409 · Cited by 161
Metadata
- Authors
- Turnbaugh, P. J., Ridaura, V. K., Faith, J. J., Rey, F. E., Knight, R., & Gordon, J. I.
- Affiliations
- Washington University in St. Louis (US)
- University of Colorado Boulder (US)
- Corresponding author
- Gordon, Jeffrey I.
- ORCID
- Venue
- Science Translational Medicine
- Published
- 2009-11-11
- Volume
- 1
- Issue
- 6
- Pages
- 6ra14-6ra14
- ISSN
- 1946-6234 (ISSN-L)
- 1946-6242
- PMC
- PMC2894525
- OpenAlex
- W2136552678
- Cited by
- 3,058
- References
- 27
- Citations by year
- 2026: 71 · 2025: 112 · 2024: 140 · 2023: 158 · 2022: 201 · 2021: 251 · 2020: 269 · 2019: 288 · 2018: 248 · 2017: 246 · 2016: 237 · 2015: 198 · 2014: 183 · 2013: 173 · 2012: 131
- FWCI
- 37.14
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science Translational Medicine (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Crohn's and Colitis Foundation
- National Institute of Diabetes and Digestive and Kidney Diseases (DK 70977, R01DK070977)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
- Keywords
- gut microbiota, diet, fecal microbiota transplantation, Western diet, high-fat high-sugar diet, bacterial colonization, intergenerational transmission, adiposity, metabolic pathways, germ-free mice, 16S rRNA gene sequences
- MeSH terms
- Animals, Bacteria, Diet, Energy Metabolism, Germ-Free Life, Humans, Intestines, Male, Mice, Inbred C57BL, Molecular Sequence Data, RNA, Ribosomal, 16S, Genomics, Adiposity, Mice
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