Abstract
A wide diversity of fungi have been detected in the human gastrointestinal (GI) tract with the potential to provide or influence important functions. However, many of the fungi most commonly detected in stool samples are also present in food or the oral cavity. Therefore, to recognize which gut fungi are likely to have a sustained influence on human health, there is a need to separate transient members of the GI tract from true colonizers. To identify colonizing fungi, the eukaryotic rRNA operon's second internal transcribed spacer (ITS2) was sequenced from the stool, saliva, and food of healthy adults following consumption of different controlled diets. Unlike most bacterial 16S rRNA genes, the only fungal ITS2 operational taxonomic units (OTUs) detected in stool DNA across multiple diets were also present in saliva and/or food. Additional analyses, including culture-based approaches and sequencing of the 18S rRNA gene, ITS2 cDNA, and DNA extracted using alternative methods, failed to detect additional fungi. Two abundant fungi, Saccharomyces cerevisiae and Candida albicans, were examined further in healthy volunteers. Saccharomyces became undetectable in stool when a S.cerevisiae-free diet was consumed, and the levels of C.albicans in stool were dramatically reduced by more frequent cleaning of teeth. Extremely low fungal abundance, the inability of fungi to grow under conditions mimicking the distal gut, and evidence from analysis of other public datasets further support the hypothesis that fungi do not routinely colonize the GI tracts of healthy adults. IMPORTANCE We sought to identify the fungi that colonize healthy GI tracts and that have a sustained influence on the diverse functions of the gut microbiome. Instead, we found that all fungi in the stool of healthy volunteers could be explained by their presence in oral and dietary sources and that our results, together with those from other analyses, support the model that there is little or no gastrointestinal colonization by fungi. This may be due to Westernization, primate evolution, fungal ecology, and/or the strong defenses of a healthy immune system. Importantly, fungal colonization of the GI tract may often be indicative of disease. As fungi can cause serious infections in immunocompromised individuals and are found at increased abundance in multiple disorders of the GI tract, understanding normal fungal colonization is essential for proper treatment and prevention of fungal pathogenesis.
Highlights
A wide diversity of fungi have been detected in the human gastrointestinal (GI) tract with the potential to provide or influence important functions
We examined the rate at which new fungal ITS2 operational taxonomic units (OTUs) could be detected in Human Microbiome Project (HMP) stool samples and compared this to the rate of detection of new 16S rRNA gene OTUs using all samples that had at least 1,000 reads from each analysis (148 shared samples from 100 volunteers)
The addition of new OTUs most closely follows a power function for ITS2 and a logarithmic curve for 16S rRNA genes. This difference in the rates of identifying new OTUs is consistent with the possibility that most of the detected fungi were derived from the consumption of different foods, which contain, as a whole, more unique microorganisms than those that may be colonizing the GI tract
Summary
A wide diversity of fungi have been detected in the human gastrointestinal (GI) tract with the potential to provide or influence important functions. The eukaryotic rRNA operon’s second internal transcribed spacer (ITS2) was sequenced from the stool, saliva, and food of healthy adults following consumption of different controlled diets. We found that all fungi in the stool of healthy volunteers could be explained by their presence in oral and dietary sources and that our results, together with those from other analyses, support the model that there is little or no gastrointestinal colonization by fungi. This may be due to Westernization, primate evolution, fungal ecology, and/or the strong defenses of a healthy immune system. Any fungal commensals possibly colonizing the GI tract may be obscured in experiments that do not control for the presence of transient fungi
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