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Diet-induced extinctions in the gut microbiota compound over generations
Open accessAbstract
The gut is home to trillions of microorganisms that have fundamental roles in many aspects of human biology, including immune function and metabolism. The reduced diversity of the gut microbiota in Western populations compared to that in populations living traditional lifestyles presents the question of which factors have driven microbiota change during modernization. Microbiota-accessible carbohydrates (MACs) found in dietary fibre have a crucial involvement in shaping this microbial ecosystem, and are notably reduced in the Western diet (high in fat and simple carbohydrates, low in fibre) compared with a more traditional diet. Here we show that changes in the microbiota of mice consuming a low-MAC diet and harbouring a human microbiota are largely reversible within a single generation. However, over several generations, a low-MAC diet results in a progressive loss of diversity, which is not recoverable after the reintroduction of dietary MACs. To restore the microbiota to its original state requires the administration of missing taxa in combination with dietary MAC consumption. Our data illustrate that taxa driven to low abundance when dietary MACs are scarce are inefficiently transferred to the next generation, and are at increased risk of becoming extinct within an isolated population. As more diseases are linked to the Western microbiota and the microbiota is targeted therapeutically, microbiota reprogramming may need to involve strategies that incorporate dietary MACs as well as taxa not currently present in the Western gut.
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In the citing paper
“An inter-generational decrease in fibre has been shown to lead to a reduction or extinction of these fibre-degrading bacteria in a mouse model [103].”
From Effect of Diet on the Gut Microbiota: Rethinking Intervention Duration (2019) · cites this paper as [103]
In the citing paper
“In contrast, multigenerational exposure to a Western diet poor in “microbiota-accessible carbohydrates” result in the extinction of specific bacterial lineages, which might negatively influence the maturation and function of the immune system, and increase the risk of developing a range of metabolic, inflammatory, allergic, and autoimmune diseases (92,94,98).”
From Health Benefits of the Mediterranean Diet: Metabolic and Molecular Mechanisms (2018) · cites this paper as [98]
In the citing paper
“Mice fed a diet low in MACs experience decreases in numerous taxa, and loss of diversity is compounded over several generations of offspring and not recovered after reintroduction of MACs (7, 9).”
From The gut microbiota at the intersection of diet and human health (2018) · cites this paper as [7]
In the citing paper
“In a multigenerational study in mice, the consumption of a Western-style diet exacerbated the loss of microbiota diversity compared with a diet that was rich in microbiota-accessible carbohydrates, and the extinction of taxa corresponded with a predicted loss in diversity of glycoside hydrolases63.”
From Diet–microbiota interactions as moderators of human metabolism (2016) · cites this paper as [63]
In the citing paper
“Low dietary fiber consumption is associated with lower microbiota diversity, fewer anti-pathogenic bacteria and less SCFA production [146], which may lead to inflammation [122] and less sympathetic nervous system stimulation [123]”
From Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes (2016) · cites this paper as [112]
In the citing paper
“As mentioned above, each dietary plan is accompanied by a simultaneous adjustment of the microbiota composition and function [112].”
From Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes (2016) · cites this paper as [112]
In the citing paper
“It is evident that the consumption of Western-style diets rich in processed, fried and sugar-rich foods and low in plant foods with their constituent fiber and polyphenols can lead to the loss of microbial diversity and function as well as the extinction of important beneficial microbes and expansion of opportunistic pathogens (13,14), with far-reaching consequences for human health.”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [13]
In the citing paper
“Long-term consumption of a Western diet in humans and animals can lead to the extinction of beneficial microbes, decrease bacterial diversity, and drive the microbiota to a predominant Bacteroides-driven enterotype (13,14,116,88).”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [13]
In the citing paper
“Studies have shown that poor dietary habits over a long period of time could lead to the potential extinction of some microbes (13,511).”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [13]
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Metadata
- Authors
- Sonnenburg, E. D., Smits, S. A., Tikhonov, M., Higginbottom, S. K., Wingreen, N. S., & Sonnenburg, J. L.
- Affiliations
- Stanford Medicine (US)
- Harvard University (US)
- Princeton University (US)
- Corresponding author
- Sonnenburg, Justin L.
- ORCID
- Venue
- Nature
- Published
- 2016-01-13
- Volume
- 529
- Issue
- 7585
- Pages
- 212-215
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4850918
- OpenAlex
- W2484230073
- Cited by
- 1,730
- References
- 26
- Citations by year
- 2026: 92 · 2025: 135 · 2024: 162 · 2023: 158 · 2022: 192 · 2021: 231 · 2020: 210 · 2019: 178 · 2018: 139 · 2017: 139 · 2016: 91
- FWCI
- 94.73
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK085025)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Health Sciences › Nursing › Nutrition and Dietetics › Microbial Metabolites in Food Biotechnology
- Keywords
- gut microbiota, dietary fiber, low-fiber diet, gut microbiota diversity, intergenerational transfers, Bacteroidales, fecal microbiota transplantation, dysbiosis, Western diet, dietary intervention, human microbiota, microbiota transfer
- MeSH terms
- Gastrointestinal Microbiome, Fecal Microbiota Transplantation, Adult, Animals, Diet, Dietary Carbohydrates, Dietary Fiber, Female, Fermentation, Germ-Free Life, Humans, Male, Pedigree, Bacteroidetes, Gastrointestinal Tract, Mice, Extinction, Biological, Healthy Volunteers
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