A Western Diet Ecological Module Identified from the ‘Humanized’ Mouse Microbiota Predicts Diet in Adults and Formula Feeding in Children

The interplay between diet and the microbiota has been implicated in the growing frequency of chronic diseases associated with the Western lifestyle. However, the complexity and variability of microbial ecology in humans and preclinical models has hampered identification of the molecular mechanisms...

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Published inPloS one Vol. 8; no. 12; p. e83689
Main Authors Siddharth, Jay, Holway, Nicholas, Parkinson, Scott J.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 31.12.2013
Public Library of Science (PLoS)
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ISSN1932-6203
1932-6203
DOI10.1371/journal.pone.0083689

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Abstract The interplay between diet and the microbiota has been implicated in the growing frequency of chronic diseases associated with the Western lifestyle. However, the complexity and variability of microbial ecology in humans and preclinical models has hampered identification of the molecular mechanisms underlying the association of the microbiota in this context. We sought to address two key questions. Can the microbial ecology of preclinical models predict human populations? And can we identify underlying principles that surpass the plasticity of microbial ecology in humans? To do this, we focused our study on diet; perhaps the most influential factor determining the composition of the gut microbiota. Beginning with a study in 'humanized' mice we identified an interactive module of 9 genera allied with Western diet intake. This module was applied to a controlled dietary study in humans. The abundance of the Western ecological module correctly predicted the dietary intake of 19/21 top and 21/21 of the bottom quartile samples inclusive of all 5 Western and 'low-fat' diet subjects, respectively. In 98 volunteers the abundance of the Western module correlated appropriately with dietary intake of saturated fatty acids, fat-soluble vitamins and fiber. Furthermore, it correlated with the geographical location and dietary habits of healthy adults from the Western, developing and third world. The module was also coupled to dietary intake in children (and piglets) correlating with formula (vs breast) feeding and associated with a precipitous development of the ecological module in young children. Our study provides a conceptual platform to translate microbial ecology from preclinical models to humans and identifies an ecological network module underlying the association of the gut microbiota with Western dietary habits.
AbstractList The interplay between diet and the microbiota has been implicated in the growing frequency of chronic diseases associated with the Western lifestyle. However, the complexity and variability of microbial ecology in humans and preclinical models has hampered identification of the molecular mechanisms underlying the association of the microbiota in this context. We sought to address two key questions. Can the microbial ecology of preclinical models predict human populations? And can we identify underlying principles that surpass the plasticity of microbial ecology in humans? To do this, we focused our study on diet; perhaps the most influential factor determining the composition of the gut microbiota. Beginning with a study in 'humanized' mice we identified an interactive module of 9 genera allied with Western diet intake. This module was applied to a controlled dietary study in humans. The abundance of the Western ecological module correctly predicted the dietary intake of 19/21 top and 21/21 of the bottom quartile samples inclusive of all 5 Western and 'low-fat' diet subjects, respectively. In 98 volunteers the abundance of the Western module correlated appropriately with dietary intake of saturated fatty acids, fat-soluble vitamins and fiber. Furthermore, it correlated with the geographical location and dietary habits of healthy adults from the Western, developing and third world. The module was also coupled to dietary intake in children (and piglets) correlating with formula (vs breast) feeding and associated with a precipitous development of the ecological module in young children. Our study provides a conceptual platform to translate microbial ecology from preclinical models to humans and identifies an ecological network module underlying the association of the gut microbiota with Western dietary habits.
The interplay between diet and the microbiota has been implicated in the growing frequency of chronic diseases associated with the Western lifestyle. However, the complexity and variability of microbial ecology in humans and preclinical models has hampered identification of the molecular mechanisms underlying the association of the microbiota in this context. We sought to address two key questions. Can the microbial ecology of preclinical models predict human populations? And can we identify underlying principles that surpass the plasticity of microbial ecology in humans? To do this, we focused our study on diet; perhaps the most influential factor determining the composition of the gut microbiota. Beginning with a study in 'humanized' mice we identified an interactive module of 9 genera allied with Western diet intake. This module was applied to a controlled dietary study in humans. The abundance of the Western ecological module correctly predicted the dietary intake of 19/21 top and 21/21 of the bottom quartile samples inclusive of all 5 Western and 'low-fat' diet subjects, respectively. In 98 volunteers the abundance of the Western module correlated appropriately with dietary intake of saturated fatty acids, fat-soluble vitamins and fiber. Furthermore, it correlated with the geographical location and dietary habits of healthy adults from the Western, developing and third world. The module was also coupled to dietary intake in children (and piglets) correlating with formula (vs breast) feeding and associated with a precipitous development of the ecological module in young children. Our study provides a conceptual platform to translate microbial ecology from preclinical models to humans and identifies an ecological network module underlying the association of the gut microbiota with Western dietary habits.The interplay between diet and the microbiota has been implicated in the growing frequency of chronic diseases associated with the Western lifestyle. However, the complexity and variability of microbial ecology in humans and preclinical models has hampered identification of the molecular mechanisms underlying the association of the microbiota in this context. We sought to address two key questions. Can the microbial ecology of preclinical models predict human populations? And can we identify underlying principles that surpass the plasticity of microbial ecology in humans? To do this, we focused our study on diet; perhaps the most influential factor determining the composition of the gut microbiota. Beginning with a study in 'humanized' mice we identified an interactive module of 9 genera allied with Western diet intake. This module was applied to a controlled dietary study in humans. The abundance of the Western ecological module correctly predicted the dietary intake of 19/21 top and 21/21 of the bottom quartile samples inclusive of all 5 Western and 'low-fat' diet subjects, respectively. In 98 volunteers the abundance of the Western module correlated appropriately with dietary intake of saturated fatty acids, fat-soluble vitamins and fiber. Furthermore, it correlated with the geographical location and dietary habits of healthy adults from the Western, developing and third world. The module was also coupled to dietary intake in children (and piglets) correlating with formula (vs breast) feeding and associated with a precipitous development of the ecological module in young children. Our study provides a conceptual platform to translate microbial ecology from preclinical models to humans and identifies an ecological network module underlying the association of the gut microbiota with Western dietary habits.
Audience Academic
Author Holway, Nicholas
Parkinson, Scott J.
Siddharth, Jay
AuthorAffiliation 1 Host Commensal Hub, Developmental and Molecular Pathways, Novartis Institutes for Biomedical Research, Basel, Switzerland
2 Scientific Computing, NIBR IT, Novartis Institutes Biomedical Research, Basel, Switzerland
Argonne National Laboratory, United States of America
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2013 Siddharth et al 2013 Siddharth et al
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Conceived and designed the experiments: JS SJP. Analyzed the data: JS NH SJP. Contributed reagents/materials/analysis tools: JS NH. Wrote the paper: SJP.
Current address: Nestle Institute of Health Sciences, Quartier de l'Innovation, EPFL, Lausanne, Switzerland
Competing Interests: All authors are employees of Novartis Institutes for Biomedical Research. This does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials.
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Snippet The interplay between diet and the microbiota has been implicated in the growing frequency of chronic diseases associated with the Western lifestyle. However,...
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SubjectTerms Abundance
Adult
Adults
Analysis
Animal models
Animals
Bacteria - classification
Bacteria - genetics
Bacteria - growth & development
Biology
Biomedical research
Bottle Feeding
Breast Feeding
Breastfeeding & lactation
Child, Preschool
Children
Children & youth
Chronic diseases
Chronic illnesses
Correlation
Datasets
Developing countries
Diet
Dietary intake
Disease
Ecological monitoring
Ecology
Fatty acids
Feces - microbiology
Feeding
Feeding Behavior
Female
Forecasts and trends
Gastrointestinal Tract - microbiology
Geographical distribution
Habits
Human populations
Humans
Infant
Infant, Newborn
Intestinal microflora
Male
Mathematical models
Medicine
Metabolism
Metagenome
Mice
Microbiota
Microbiota (Symbiotic organisms)
Microorganisms
Molecular modelling
Nutrition research
Obesity
RNA, Ribosomal, 16S - genetics
Studies
Vitamins
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Title A Western Diet Ecological Module Identified from the ‘Humanized’ Mouse Microbiota Predicts Diet in Adults and Formula Feeding in Children
URI https://www.ncbi.nlm.nih.gov/pubmed/24391809
https://www.proquest.com/docview/1473341113
https://www.proquest.com/docview/1490747863
https://pubmed.ncbi.nlm.nih.gov/PMC3877084
https://doaj.org/article/434f75e71dc54600b974d8678492512c
http://dx.doi.org/10.1371/journal.pone.0083689
Volume 8
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