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 in | PloS one Vol. 8; no. 12; p. e83689 |
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Main Authors | , , |
Format | Journal Article |
Language | English |
Published |
United States
Public Library of Science
31.12.2013
Public Library of Science (PLoS) |
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Online Access | Get full text |
ISSN | 1932-6203 1932-6203 |
DOI | 10.1371/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. |
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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 |
AuthorAffiliation_xml | – name: 1 Host Commensal Hub, Developmental and Molecular Pathways, Novartis Institutes for Biomedical Research, Basel, Switzerland – name: Argonne National Laboratory, United States of America – name: 2 Scientific Computing, NIBR IT, Novartis Institutes Biomedical Research, Basel, Switzerland |
Author_xml | – sequence: 1 givenname: Jay surname: Siddharth fullname: Siddharth, Jay – sequence: 2 givenname: Nicholas surname: Holway fullname: Holway, Nicholas – sequence: 3 givenname: Scott J. surname: Parkinson fullname: Parkinson, Scott J. |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24391809$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1128_mBio_01785_15 crossref_primary_10_1016_j_neulet_2019_134297 crossref_primary_10_1371_journal_pone_0102649 crossref_primary_10_1016_j_jcmgh_2014_11_004 crossref_primary_10_1155_2016_6787269 crossref_primary_10_1186_s12967_017_1175_y crossref_primary_10_1177_0023677218787554 crossref_primary_10_1186_s12866_021_02106_4 crossref_primary_10_3390_microorganisms13020305 crossref_primary_10_3390_ijms150711678 crossref_primary_10_3389_fcimb_2021_650893 crossref_primary_10_3389_fmicb_2019_00390 |
Cites_doi | 10.1128/AEM.02810-10 10.1126/science.1153527 10.1136/bmj.c5955 10.1093/ajcn/85.6.1457 10.1038/nature09944 10.1371/journal.pone.0030273 10.1126/science.1208344 10.1126/scitranslmed.3004347 10.1128/AEM.01541-09 10.1146/annurev.micro.030608.101423 10.1073/pnas.1102938108 10.1126/science.336.6086.1250 10.1038/nature11053 10.1093/ajcn/34.2.252 |
ContentType | Journal Article |
Copyright | COPYRIGHT 2013 Public Library of Science 2013 Siddharth et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2013 Siddharth et al 2013 Siddharth et al |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 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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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 |
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