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      Archaea and Fungi of the Human Gut Microbiome: Correlations with Diet and Bacterial Residents

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          Abstract

          Diet influences health as a source of nutrients and toxins, and by shaping the composition of resident microbial populations. Previous studies have begun to map out associations between diet and the bacteria and viruses of the human gut microbiome. Here we investigate associations of diet with fungal and archaeal populations, taking advantage of samples from 98 well-characterized individuals. Diet was quantified using inventories scoring both long-term and recent diet, and archaea and fungi were characterized by deep sequencing of marker genes in DNA purified from stool. For fungi, we found 66 genera, with generally mutually exclusive presence of either the phyla Ascomycota or Basiodiomycota. For archaea, Methanobrevibacter was the most prevalent genus, present in 30% of samples. Several other archaeal genera were detected in lower abundance and frequency. Myriad associations were detected for fungi and archaea with diet, with each other, and with bacterial lineages. Methanobrevibacter and Candida were positively associated with diets high in carbohydrates, but negatively with diets high in amino acids, protein, and fatty acids. A previous study emphasized that bacterial population structure was associated primarily with long-term diet, but high Candida abundance was most strongly associated with the recent consumption of carbohydrates. Methobrevibacter abundance was associated with both long term and recent consumption of carbohydrates. These results confirm earlier targeted studies and provide a host of new associations to consider in modeling the effects of diet on the gut microbiome and human health.

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          Most cited references61

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          QIIME allows analysis of high-throughput community sequencing data.

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            Human gut microbiome viewed across age and geography

            Gut microbial communities represent one source of human genetic and metabolic diversity. To examine how gut microbiomes differ between human populations when viewed from the perspective of component microbial lineages, encoded metabolic functions, stage of postnatal development, and environmental exposures, we characterized bacterial species present in fecal samples obtained from 531 individuals representing healthy Amerindians from the Amazonas of Venezuela, residents of rural Malawian communities, and inhabitants of USA metropolitan areas, as well as the gene content of 110 of their microbiomes. This cohort encompassed infants, children, teenagers and adults, parents and offspring, and included mono- and dizygotic twins. Shared features of the functional maturation of the gut microbiome were identified during the first three years of life in all three populations, including age-associated changes in the representation of genes involved in vitamin biosynthesis and metabolism. Pronounced differences in bacterial species assemblages and functional gene repertoires were noted between individuals residing in the USA compared to the other two countries. These distinctive features are evident in early infancy as well as adulthood. In addition, the similarity of fecal microbiomes among family members extends across cultures. These findings underscore the need to consider the microbiome when evaluating human development, nutritional needs, physiological variations, and the impact of Westernization.
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              Enterotypes of the human gut microbiome.

              Our knowledge of species and functional composition of the human gut microbiome is rapidly increasing, but it is still based on very few cohorts and little is known about variation across the world. By combining 22 newly sequenced faecal metagenomes of individuals from four countries with previously published data sets, here we identify three robust clusters (referred to as enterotypes hereafter) that are not nation or continent specific. We also confirmed the enterotypes in two published, larger cohorts, indicating that intestinal microbiota variation is generally stratified, not continuous. This indicates further the existence of a limited number of well-balanced host-microbial symbiotic states that might respond differently to diet and drug intake. The enterotypes are mostly driven by species composition, but abundant molecular functions are not necessarily provided by abundant species, highlighting the importance of a functional analysis to understand microbial communities. Although individual host properties such as body mass index, age, or gender cannot explain the observed enterotypes, data-driven marker genes or functional modules can be identified for each of these host properties. For example, twelve genes significantly correlate with age and three functional modules with the body mass index, hinting at a diagnostic potential of microbial markers.

                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                17 June 2013
                : 8
                : 6
                : e66019
                Affiliations
                [1 ]Department of Microbiology, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America
                [2 ]Division of Gastroenterology, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America
                [3 ]Center for Clinical Epidemiology and Biostatistics, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America
                [4 ]Department of Biostatistics and Epidemiology, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America
                [5 ]Instituto de Ciências Biológicas, Universidade Federal de Goiás, Goiania, Goiás, Brazil
                [6 ]Department of Biostatistics, Harvard School of Public Health, Boston, Massachusetts, United States of America
                Oak Ridge National Lab, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: CH GDW JDL FDB. Performed the experiments: CH SD SG. Analyzed the data: CH JC HL. Wrote the paper: CH FDB.

                Article
                PONE-D-13-08118
                10.1371/journal.pone.0066019
                3684604
                23799070
                e3b3419e-5530-419c-bfd9-3c70226a7fda
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 22 February 2013
                : 30 April 2013
                Page count
                Pages: 12
                Funding
                This work was supported by Project UH2/3 DK083981, the Penn Genome Frontiers Institute; National Institutes of Health (NIH) DK 089472 (GDW); Penn Digestive Disease Center (P30 DK050306); The Joint Penn-CHOP Center for Digestive, Liver, and Pancreatic Medicine; S10RR024525; UL1RR024134, and K24-DK078228. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Center for Research Resources, National Institutes of Health, or Pennsylvania Department of Health. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Computational Biology
                Sequence Analysis
                Genomics
                Metagenomics
                Microbiology
                Mycology
                Fungi
                Archaeans
                Microbial Ecology
                Microbial Metabolism
                Medicine
                Clinical Research Design
                Cross-Sectional Studies
                Nutrition
                Pediatrics
                Neonatology

                Uncategorized
                Uncategorized

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