Microbial co-occurrence relationships in the human microbiome
Open accessAbstract
The healthy microbiota show remarkable variability within and among individuals. In addition to external exposures, ecological relationships (both oppositional and symbiotic) between microbial inhabitants are important contributors to this variation. It is thus of interest to assess what relationships might exist among microbes and determine their underlying reasons. The initial Human Microbiome Project (HMP) cohort, comprising 239 individuals and 18 different microbial habitats, provides an unprecedented resource to detect, catalog, and analyze such relationships. Here, we applied an ensemble method based on multiple similarity measures in combination with generalized boosted linear models (GBLMs) to taxonomic marker (16S rRNA gene) profiles of this cohort, resulting in a global network of 3,005 significant co-occurrence and co-exclusion relationships between 197 clades occurring throughout the human microbiome. This network revealed strong niche specialization, with most microbial associations occurring within body sites and a number of accompanying inter-body site relationships. Microbial communities within the oropharynx grouped into three distinct habitats, which themselves showed no direct influence on the composition of the gut microbiota. Conversely, niches such as the vagina demonstrated little to no decomposition into region-specific interactions. Diverse mechanisms underlay individual interactions, with some such as the co-exclusion of Porphyromonaceae family members and Streptococcus in the subgingival plaque supported by known biochemical dependencies. These differences varied among broad phylogenetic groups as well, with the Bacilli and Fusobacteria, for example, both enriched for exclusion of taxa from other clades. Comparing phylogenetic versus functional similarities among bacteria, we show that dominant commensal taxa (such as Prevotellaceae and Bacteroides in the gut) often compete, while potential pathogens (e.g. Treponema and Prevotella in the dental plaque) are more likely to co-occur in complementary niches. This approach thus serves to open new opportunities for future targeted mechanistic studies of the microbial ecology of the human microbiome.
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Bacteroides and Prevotella are taxonomically and functionally similar yet do not co-exist in the intestine, possibly because of competition within the same niche.
“However, Bacteroides and Prevotella are taxonomically and functionally similar genera, yet do not co-exist in the intestine; this is an exception to the model, possibly resulting from competition within the same niche41.”
From Diet and the Intestinal Microbiome: Associations, Functions, and Implications for Health and Disease (2014) · cites this paper as [41]
A better term may be enterogradient, based on whether Bacteroides or Prevotella dominate, because these two genera generally do not exist in equal proportions in the human intestine.
“A better term might be enterogradient, based on whether Bacteroides or Prevotella dominate the intestinal microbial community—it appears that these 2 genera generally do not exist in equal proportions in the human intestine 41.”
From Diet and the Intestinal Microbiome: Associations, Functions, and Implications for Health and Disease (2014) · cites this paper as [41]
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- Authors
- Faust, K., Sathirapongsasuti, J. F., Izard, J., Segata, N., Gevers, D., Raes, J., & Huttenhower, C.
- Affiliations
- Vrije Universiteit Brussel (BE)
- Harvard University (US)
- Broad Institute (US)
- Corresponding author
- Faust, Karoline
- Sathirapongsasuti, J. Fah
- Izard, Jacques
- Segata, Nicola
- Gevers, Dirk
- Raes, Jeroen
- Huttenhower, Curtis
- ORCID
- Venue
- PLoS Computational Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-07-12
- Volume
- 8
- Issue
- 7
- Pages
- e1002606
- ISSN
- 1553-734X (ISSN-L)
- 1553-7358
- PMC
- PMC3395616
- OpenAlex
- W1971061059
- Cited by
- 1,527
- References
- 85
- Citations by year
- 2026: 64 · 2025: 97 · 2024: 99 · 2023: 115 · 2022: 124 · 2021: 168 · 2020: 169 · 2019: 117 · 2018: 114 · 2017: 133 · 2016: 116 · 2015: 92 · 2014: 58 · 2013: 48 · 2012: 11
- FWCI
- 26.89
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Computational Biology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- Lincoln (University of Nebraska) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Figshare (submittedVersion, cc-by)
- Institutional Research Information System (Università degli Studi di Trento) (submittedVersion)
- VUBIR (Vrije Universiteit Brussel) (submittedVersion)
- Funders
- National Science Foundation (1053486)
- Crohn's and Colitis Foundation of America
- Crohn's and Colitis Foundation
- Fonds Wetenschappelijk Onderzoek
- Vlaamse regering
- National Institutes of Health (ARO W911NF-11-1-0473, DBI-1053486)
- National Human Genome Research Institute (U54HG004969, R01HG005969)
- National Cancer Institute (R21CA139193, CA139193)
- National Institute of Diabetes and Digestive and Kidney Diseases (P30DK043351)
- Division of Biological Infrastructure (DBI-1053486)
- Army Research Office (W911NF-11-1-0473, W911NF, W911NF-11)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Keywords
- microbial co-occurrence networks, human microbiome, oropharyngeal microbiota, gut microbiota, vaginal microbiota, subgingival plaque, Streptococcus, Fusobacteria, bacilli, Prevotella, Bacteroides, Treponema
- MeSH terms
- Bacteria, DNA, Bacterial, Female, Humans, Male, Nasal Cavity, Phylogeny, Skin, Vagina, Linear Models, Ecosystem, Bacterial Physiological Phenomena, Computational Biology, Genes, rRNA, Gastrointestinal Tract, Metagenome, Microbial Interactions
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