Caloric restriction disrupts the microbiota and colonization resistance

Diet is a major factor that shapes the gut microbiome 1 , but the consequences of diet-induced changes in the microbiome for host pathophysiology remain poorly understood. We conducted a randomized human intervention study using a very-low-calorie diet (NCT01105143). Although metabolic health was im...

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Published inNature (London) Vol. 595; no. 7866; pp. 272 - 277
Main Authors von Schwartzenberg, Reiner Jumpertz, Bisanz, Jordan E., Lyalina, Svetlana, Spanogiannopoulos, Peter, Ang, Qi Yan, Cai, Jingwei, Dickmann, Sophia, Friedrich, Marie, Liu, Su-Yang, Collins, Stephanie L., Ingebrigtsen, Danielle, Miller, Steve, Turnbaugh, Jessie A., Patterson, Andrew D., Pollard, Katherine S., Mai, Knut, Spranger, Joachim, Turnbaugh, Peter J.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 08.07.2021
Nature Publishing Group
Subjects
38
45
45/23
631/326/2565/2134
631/443/319/1642/2037
64
64/60
692/700/2814
Adipose tissue
Adiposity
Animals
Bacteria
Bacteria - growth & development
Bacteria - isolation & purification
Bacteria - metabolism
Bacteria - pathogenicity
Bacterial Toxins - metabolism
Bile acids
Bile Acids and Salts - metabolism
Body Weight
Body weight loss
Caloric Restriction
Calories
Clostridioides difficile - growth & development
Clostridioides difficile - isolation & purification
Clostridioides difficile - metabolism
Colonization
Diet
Diet, Reducing
Dietary restrictions
Energy balance
Energy Metabolism
Enzymes
Gastrointestinal Microbiome - physiology
Genes
Glucose
Humanities and Social Sciences
Humans
Hypocaloric diet
Intestinal Absorption
Intestinal microflora
Male
Metabolism
Mice
Microbiomes
Microbiota
multidisciplinary
Nutrient deficiency
Nutrient loss
Nutrients - metabolism
Phenotypes
Science
Science (multidisciplinary)
Symbionts
Symbiosis
Toxins
Transplantation
Weight control
Weight Loss
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Abstract Diet is a major factor that shapes the gut microbiome 1 , but the consequences of diet-induced changes in the microbiome for host pathophysiology remain poorly understood. We conducted a randomized human intervention study using a very-low-calorie diet (NCT01105143). Although metabolic health was improved, severe calorie restriction led to a decrease in bacterial abundance and restructuring of the gut microbiome. Transplantation of post-diet microbiota to mice decreased their body weight and adiposity relative to mice that received pre-diet microbiota. Weight loss was associated with impaired nutrient absorption and enrichment in Clostridioides difficile , which was consistent with a decrease in bile acids and was sufficient to replicate metabolic phenotypes in mice in a toxin-dependent manner. These results emphasize the importance of diet–microbiome interactions in modulating host energy balance and the need to understand the role of diet in the interplay between pathogenic and beneficial symbionts. Severe caloric restriction in humans leads to reversible changes in the gut microbiota that promote weight loss and the expansion of an enteric pathogen in mice.
AbstractList Diet is a major factor that shapes the gut microbiome 1 , but the consequences of diet-induced changes in the microbiome for host pathophysiology remain poorly understood. We conducted a randomized human intervention study using a very-low-calorie diet (NCT01105143). Although metabolic health was improved, severe calorie restriction led to a decrease in bacterial abundance and restructuring of the gut microbiome. Transplantation of post-diet microbiota to mice decreased their body weight and adiposity relative to mice that received pre-diet microbiota. Weight loss was associated with impaired nutrient absorption and enrichment in Clostridioides difficile , which was consistent with a decrease in bile acids and was sufficient to replicate metabolic phenotypes in mice in a toxin-dependent manner. These results emphasize the importance of diet–microbiome interactions in modulating host energy balance and the need to understand the role of diet in the interplay between pathogenic and beneficial symbionts. Severe caloric restriction in humans leads to reversible changes in the gut microbiota that promote weight loss and the expansion of an enteric pathogen in mice.
Diet is a major factor that shapes the gut microbiome , but the consequences of diet-induced changes in the microbiome for host pathophysiology remain poorly understood. We conducted a randomized human intervention study using a very-low-calorie diet (NCT01105143). Although metabolic health was improved, severe calorie restriction led to a decrease in bacterial abundance and restructuring of the gut microbiome. Transplantation of post-diet microbiota to mice decreased their body weight and adiposity relative to mice that received pre-diet microbiota. Weight loss was associated with impaired nutrient absorption and enrichment in Clostridioides difficile, which was consistent with a decrease in bile acids and was sufficient to replicate metabolic phenotypes in mice in a toxin-dependent manner. These results emphasize the importance of diet-microbiome interactions in modulating host energy balance and the need to understand the role of diet in the interplay between pathogenic and beneficial symbionts.
Diet is a major factor that shapes the gut microbiome 1 , but the consequences of diet-induced microbiome shifts for host pathophysiology remain poorly understood. We conducted a randomized human intervention study using very-low calorie diets (VLCD). While metabolic health was improved, severe calorie restriction led to decreased bacterial abundance and restructuring of the gut microbiome. Transplantation of post-diet microbiotas to mice decreased body weight and adiposity relative to pre-diet microbiota recipients. Weight loss was associated with impaired nutrient absorption and an enrichment of Clostridioides difficile , which was consistent with a decrease in bile acids and sufficient to replicate metabolic phenotypes in mice in a toxin-dependent manner. These results emphasize the importance of diet-microbiome interactions in modulating host energy balance and the need to understand the role of diet in the interplay between pathogenic and beneficial symbionts.
Diet is a major factor that shapes the gut microbiome1, but the consequences of diet-induced changes in the microbiome for host pathophysiology remain poorly understood. We conducted a randomized human intervention study using a very-low-calorie diet (NCT01105143). Although metabolic health was improved, severe calorie restriction led to a decrease in bacterial abundance and restructuring of the gut microbiome. Transplantation of post-diet microbiota to mice decreased their body weight and adiposity relative to mice that received pre-diet microbiota. Weight loss was associated with impaired nutrient absorption and enrichment in Clostridioides difficile, which was consistent with a decrease in bile acids and was sufficient to replicate metabolic phenotypes in mice in a toxin-dependent manner. These results emphasize the importance of diet-microbiome interactions in modulating host energy balance and the need to understand the role of diet in the interplay between pathogenic and beneficial symbionts.
Diet is a major factor that shapes the gut microbiome1, but the consequences of diet-induced changes in the microbiome for host pathophysiology remain poorly understood. We conducted a randomized human intervention study using a very-low-calorie diet (NCT01105143). Although metabolic health was improved, severe calorie restriction led to a decrease in bacterial abundance and restructuring of the gut microbiome. Transplantation of post-diet microbiota to mice decreased their body weight and adiposity relative to mice that received pre-diet microbiota. Weight loss was associated with impaired nutrient absorption and enrichment in Clostridioides difficile, which was consistent with a decrease in bile acids and was sufficient to replicate metabolic phenotypes in mice in a toxin-dependent manner. These results emphasize the importance of diet-microbiome interactions in modulating host energy balance and the need to understand the role of diet in the interplay between pathogenic and beneficial symbionts.Diet is a major factor that shapes the gut microbiome1, but the consequences of diet-induced changes in the microbiome for host pathophysiology remain poorly understood. We conducted a randomized human intervention study using a very-low-calorie diet (NCT01105143). Although metabolic health was improved, severe calorie restriction led to a decrease in bacterial abundance and restructuring of the gut microbiome. Transplantation of post-diet microbiota to mice decreased their body weight and adiposity relative to mice that received pre-diet microbiota. Weight loss was associated with impaired nutrient absorption and enrichment in Clostridioides difficile, which was consistent with a decrease in bile acids and was sufficient to replicate metabolic phenotypes in mice in a toxin-dependent manner. These results emphasize the importance of diet-microbiome interactions in modulating host energy balance and the need to understand the role of diet in the interplay between pathogenic and beneficial symbionts.
Author Pollard, Katherine S.
Miller, Steve
Cai, Jingwei
Spranger, Joachim
Collins, Stephanie L.
Ingebrigtsen, Danielle
Friedrich, Marie
Turnbaugh, Jessie A.
Patterson, Andrew D.
Turnbaugh, Peter J.
von Schwartzenberg, Reiner Jumpertz
Dickmann, Sophia
Liu, Su-Yang
Lyalina, Svetlana
Bisanz, Jordan E.
Mai, Knut
Spanogiannopoulos, Peter
Ang, Qi Yan
AuthorAffiliation 7 Department of Pathology, University of California San Francisco, 513 Parnassus Avenue, San Francisco, CA 94143, USA
5 Gladstone Institutes, 1650 Owens Street, San Francisco, CA 94158, USA
3 DZHK (German Centre for Cardiovascular Research), partner site Berlin, Center for Cardiovascular Research (CCR), Berlin, Germany
2 Berlin Institute of Health (BIH), Anna-Louisa-Karsch-Straße 2, 10178 Berlin, Germany
4 Department of Microbiology & Immunology, University of California San Francisco, 513 Parnassus Avenue, San Francisco, CA 94143, USA
9 Department of Epidemiology & Biostatistics, Institute for Human Genetics, and Institute for Computational Health Sciences, University of California San Francisco, CA 94158, USA
10 Chan Zuckerberg Biohub, San Francisco, CA 94158, USA
1 Charité Universitätsmedizin Berlin, Department of Endocrinology and Metabolic Diseases, Charitéplatz 1, 10117 Berlin, Germany
6 Center for Molecular Toxicology and Carcinogenesis, Department of Veterinary and Biomedical Sciences,
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  organization: Department of Microbiology & Immunology, University of California San Francisco
BackLink https://www.ncbi.nlm.nih.gov/pubmed/34163067$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright The Author(s), under exclusive licence to Springer Nature Limited 2021
Copyright Nature Publishing Group Jul 8, 2021
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– notice: Copyright Nature Publishing Group Jul 8, 2021
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Manuscript preparation with input from all authors: JEB, RJvS, JS, and PJT. Human cohort design and execution RJvS, KM, and JS. Microbiome transplantation experiment design and execution: JEB, RJvS, PS, QYA, SD, MF, JAT, JS, and PJT. 16S rRNA gene sequencing and analysis: JEB, RJvS, and PS. Metagenomic sequencing and analysis: JEB, SL, RJvS, and KSP. Metabolomic quantification and analysis: JC, JEB, SLC, and ADP. C. difficile in vitro and gnotobiotic experiments: JEB, JAT, and PJT. Histological scoring: S-YL. C. difficile testing: JEB, DI, SM. Statistical analysis and data presentation: JEB, RJvS, SL, KSP, and PJT. Supervision and funding: RJvS, ADP, KSP, KM, JS, and PJT.
These authors contributed equally
Author contributions
ORCID 0000-0002-9870-6196
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0000-0002-8900-4467
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0000-0002-8649-1706
0000-0002-9788-1283
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Snippet Diet is a major factor that shapes the gut microbiome 1 , but the consequences of diet-induced changes in the microbiome for host pathophysiology remain poorly...
Diet is a major factor that shapes the gut microbiome , but the consequences of diet-induced changes in the microbiome for host pathophysiology remain poorly...
Diet is a major factor that shapes the gut microbiome1, but the consequences of diet-induced changes in the microbiome for host pathophysiology remain poorly...
Diet is a major factor that shapes the gut microbiome 1 , but the consequences of diet-induced microbiome shifts for host pathophysiology remain poorly...
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SubjectTerms 38
45
45/23
631/326/2565/2134
631/443/319/1642/2037
64
64/60
692/700/2814
Adipose tissue
Adiposity
Animals
Bacteria
Bacteria - growth & development
Bacteria - isolation & purification
Bacteria - metabolism
Bacteria - pathogenicity
Bacterial Toxins - metabolism
Bile acids
Bile Acids and Salts - metabolism
Body Weight
Body weight loss
Caloric Restriction
Calories
Clostridioides difficile - growth & development
Clostridioides difficile - isolation & purification
Clostridioides difficile - metabolism
Colonization
Diet
Diet, Reducing
Dietary restrictions
Energy balance
Energy Metabolism
Enzymes
Gastrointestinal Microbiome - physiology
Genes
Glucose
Humanities and Social Sciences
Humans
Hypocaloric diet
Intestinal Absorption
Intestinal microflora
Male
Metabolism
Mice
Microbiomes
Microbiota
multidisciplinary
Nutrient deficiency
Nutrient loss
Nutrients - metabolism
Phenotypes
Science
Science (multidisciplinary)
Symbionts
Symbiosis
Toxins
Transplantation
Weight control
Weight Loss
Title Caloric restriction disrupts the microbiota and colonization resistance
URI https://link.springer.com/article/10.1038/s41586-021-03663-4
https://www.ncbi.nlm.nih.gov/pubmed/34163067
https://www.proquest.com/docview/2549731647
https://www.proquest.com/docview/2544880239
https://pubmed.ncbi.nlm.nih.gov/PMC8959578
Volume 595
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