Dataset Information

Microbial co-occurrence relationships in the human microbiome.

ABSTRACT: 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.

SUBMITTER: Faust K

PROVIDER: S-EPMC3395616 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Microbial co-occurrence relationships in the human microbiome.

Faust Karoline K Sathirapongsasuti J Fah JF Izard Jacques J Segata Nicola N Gevers Dirk D Raes Jeroen J Huttenhower Curtis C

PLoS computational biology 20120712 7

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 unp ...[more]

PMID: 22807668

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Project description:Drawing on a long history in macroecology, correlation analysis of microbiome datasets is becoming a common practice for identifying relationships or shared ecological niches among bacterial taxa. However, many of the statistical issues that plague such analyses in macroscale communities remain unresolved for microbial communities. Here, we discuss problems in the analysis of microbial species correlations based on presence-absence data. We focus on presence-absence data because this information is more readily obtainable from sequencing studies, especially for whole-genome sequencing, where abundance estimation is still in its infancy. First, we show how Pearson's correlation coefficient (r) and Jaccard's index (J)-two of the most common metrics for correlation analysis of presence-absence data-can contradict each other when applied to a typical microbiome dataset. In our dataset, for example, 14% of species-pairs predicted to be significantly correlated by r were not predicted to be significantly correlated using J, while 37.4% of species-pairs predicted to be significantly correlated by J were not predicted to be significantly correlated using r. Mismatch was particularly common among species-pairs with at least one rare species (<10% prevalence), explaining why r and J might differ more strongly in microbiome datasets, where there are large numbers of rare taxa. Indeed 74% of all species-pairs in our study had at least one rare species. Next, we show how Pearson's correlation coefficient can result in artificial inflation of positive taxon relationships and how this is a particular problem for microbiome studies. We then illustrate how Jaccard's index of similarity (J) can yield improvements over Pearson's correlation coefficient. However, the standard null model for Jaccard's index is flawed, and thus introduces its own set of spurious conclusions. We thus identify a better null model based on a hypergeometric distribution, which appropriately corrects for species prevalence. This model is available from recent statistics literature, and can be used for evaluating the significance of any value of an empirically observed Jaccard's index. The resulting simple, yet effective method for handling correlation analysis of microbial presence-absence datasets provides a robust means of testing and finding relationships and/or shared environmental responses among microbial taxa.

Dataset Information

Microbial co-occurrence relationships in the human microbiome.

Publications

Microbial co-occurrence relationships in the human microbiome.

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