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Cited by 815Gut microbiota and healthGastrointestinal motility and disordersMicrobial Community Ecology and Physiology

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

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Hoffmann, Christian, Dollive, Serena, Grunberg, Stephanie, Chen, Jun, Li, Hongzhe, Wu, Gary D., Lewis, James D., Bushman, Frederic D.·2013·PLoS ONE
DOI 10.1371/journal.pone.0066019PMC PMC3684604
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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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Figures

Figure 1 The archaeal and fungal components of the human gut microbiome. The heatmaps show the relative proportions of microbial lineages detected by pyrosequencing. The lineages are marked on the right, with Phylum (abbreviated), Class, and Genus. Archaeal genera are shown in (A), representative bacterial genera in (B), and fungal genera in (C). The top two rows show the DNA yield from PCR amplification reactions, which serves as a rough indicator of abundance. Proportions were calculated within each amplicon (archaeal 16S, bacterial 16S, or fungal ITS) for each sequencing study separately. The abbreviations for phyla were as follows (Eur: Euryarchaeota; Tha: Thaumarchaeota; Act: Actinobacteria; Bac: Bacteroidetes; Fir: Firmicutes; Asc: Ascomycota; Bas; Basidiomycota). Other Ascomycota and Other Basidiomycota are composed of genera which were detected in only one sample (see Table S7 and Figure S2 for a complete list of detected genera and their prevalence).
Figure 1 The archaeal and fungal components of the human gut microbiome. The heatmaps show the relative proportions of microbial lineages detected by pyrosequencing. The lineages are marked on the right, with Phylum (abbreviated), Class, and Genus. Archaeal genera are shown in (A), representative bacterial genera in (B), and fungal genera in (C). The top two rows show the DNA yield from PCR amplification reactions, which serves as a rough indicator of abundance. Proportions were calculated within each amplicon (archaeal 16S, bacterial 16S, or fungal ITS) for each sequencing study separately. The abbreviations for phyla were as follows (Eur: Euryarchaeota; Tha: Thaumarchaeota; Act: Actinobacteria; Bac: Bacteroidetes; Fir: Firmicutes; Asc: Ascomycota; Bas; Basidiomycota). Other Ascomycota and Other Basidiomycota are composed of genera which were detected in only one sample (see Table S7 and Figure S2 for a complete list of detected genera and their prevalence).CC BY · PubMed Central
Figure 2 Analysis of co-occurrence among microbial lineages scored using the Dice index. Dice indexes across all genera pairs present at a proportion > = 0.01 are shown as a heatmap. Clustering was carried out using Ward’s criteria, based on the Euclidian distance between each genus pair using their Dice index across all other genera. Domain membership is color-coded on the left. Data are summarized in Table S9 and S10.
Figure 2 Analysis of co-occurrence among microbial lineages scored using the Dice index. Dice indexes across all genera pairs present at a proportion > = 0.01 are shown as a heatmap. Clustering was carried out using Ward’s criteria, based on the Euclidian distance between each genus pair using their Dice index across all other genera. Domain membership is color-coded on the left. Data are summarized in Table S9 and S10.CC BY · PubMed Central
Figure 3 Inter-generic relationships. The heatmaps quantify the intergeneric relationships. (A) Normalized z-score of the bacterial and fungal proportions for samples grouped according to their archaeal status (Methanobrevibacter positive, Nitrososphaera positive, or archaea negative). Asterisks indicate Kruskall-Wallis significant comparisons after FDR adjustment (FDR of 25, 20, 15, and 10% are marked with 1, 2, 3 or 4 asterisks, respectively). Domain membership is color-coded on the left. (B) Spearman correlations between Fungi and Bacteria. Asterisks in red indicate FDR adjusted significant correlations (FDR 20%) and the remaining raw p-values are shown to illustrate general patterns within the data (p-values < = 0.05, 0.01, 0.005, 0.001 are marked with 1, 2, 3 or 4 asterisks, respectively).
Figure 3 Inter-generic relationships. The heatmaps quantify the intergeneric relationships. (A) Normalized z-score of the bacterial and fungal proportions for samples grouped according to their archaeal status (Methanobrevibacter positive, Nitrososphaera positive, or archaea negative). Asterisks indicate Kruskall-Wallis significant comparisons after FDR adjustment (FDR of 25, 20, 15, and 10% are marked with 1, 2, 3 or 4 asterisks, respectively). Domain membership is color-coded on the left. (B) Spearman correlations between Fungi and Bacteria. Asterisks in red indicate FDR adjusted significant correlations (FDR 20%) and the remaining raw p-values are shown to illustrate general patterns within the data (p-values < = 0.05, 0.01, 0.005, 0.001 are marked with 1, 2, 3 or 4 asterisks, respectively).CC BY · PubMed Central
Figure 4 Archaea-Diet relationships. Heatmap of normalized average means for nutrient cluster measurements of the samples classified according to the dominant archaeal genus. Usual diet (A) and recent diet (B) relationships considered significant are marked with asterisks as described in Figure 2A.
Figure 4 Archaea-Diet relationships. Heatmap of normalized average means for nutrient cluster measurements of the samples classified according to the dominant archaeal genus. Usual diet (A) and recent diet (B) relationships considered significant are marked with asterisks as described in Figure 2A.CC BY · PubMed Central
Figure 5 Fungi-Diet relationships. Heatmap of Spearman correlations between nutrient clusters and the bacterial and fungal genera detected in the dataset. Correlations which were considered significant using the Usual (A) and the Recent (B) diet data are marked with asterisks as in Figure 2A. Domain membership is color-coded on the bottom.
Figure 5 Fungi-Diet relationships. Heatmap of Spearman correlations between nutrient clusters and the bacterial and fungal genera detected in the dataset. Correlations which were considered significant using the Usual (A) and the Recent (B) diet data are marked with asterisks as in Figure 2A. Domain membership is color-coded on the bottom.CC BY · PubMed Central
Figure 6 Possible syntrophic relationships in the human gut consistent with data reported in this study.
Figure 6 Possible syntrophic relationships in the human gut consistent with data reported in this study.CC BY · PubMed Central

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Metadata

Authors
Hoffmann, C., Dollive, S., Grunberg, S., Chen, J., Li, H., Wu, G. D., Lewis, J. D., & Bushman, F. D.
Affiliations
  • Universidade Federal de Goiás (BR)
  • University of Pennsylvania (US)
  • Harvard University (US)
Corresponding author
  • Wu, Gary D.
  • Lewis, James D.
  • Bushman, Frederic D.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2013-06-17
Volume
8
Issue
6
Pages
e66019
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0066019
PMC
PMC3684604
OpenAlex
W2110345840
Cited by
808
References
62
Citations by year
2026: 38 · 2025: 56 · 2024: 73 · 2023: 59 · 2022: 86 · 2021: 85 · 2020: 87 · 2019: 76 · 2018: 60 · 2017: 62 · 2016: 36 · 2015: 45 · 2014: 40 · 2013: 4
FWCI
18.65
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • Pennsylvania Department of Health
  • University of Pennsylvania (UL1 RR024134)
  • National Institutes of Health (and K24, DK050306)
  • National Institute of Diabetes and Digestive and Kidney Diseases (K24DK078228, DK 089472, R01DK089472, UH2/3 DK083981, UH3DK083981, UH2DK083981, P30DK050306)
  • National Center for Research Resources (UL1RR024134, S10RR024525)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Keywords
gut microbiota, archaea, fungi, diet, Methanobrevibacter, Candida, Ascomycota, carbohydrate intake, long-term diet, microbial co-occurrence, human health
MeSH terms
Archaea, Bacteria, Diet, Fungi, Humans, Intestines, Microbiota

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