Abstract
Archaea are habitual residents of the human gut flora but are detected at substantially lower frequencies than bacteria. Previous studies have indicated that each human harbors very few archaeal species. However, the low diversity of human-associated archaea that has been detected could be due to the preponderance of bacteria in these communities, such that relatively few sequences are classified as Archaea even when microbiomes are sampled deeply. Moreover, the universal prokaryotic primer pair typically used to interrogate microbial diversity has low specificity to the archaeal domain, potentially leaving vast amounts of diversity unobserved. As a result, the prevalence, diversity, and distribution of archaea may be substantially underestimated. Here we evaluate archaeal diversity in gut microbiomes using an approach that targets virtually all known members of this domain. Comparing microbiomes across five great ape species allowed us to examine the dynamics of archaeal lineages over evolutionary time scales. These analyses revealed hundreds of gut-associated archaeal lineages, indicating that upwards of 90% of the archaeal diversity in the human and great ape gut microbiomes has been overlooked. Additionally, these results indicate a progressive reduction in archaeal diversity in the human lineage, paralleling the decline reported for bacteria. IMPORTANCE Our findings show that Archaea are a habitual and vital component of human and great ape gut microbiomes but are largely ignored on account of the failure of previous studies to realize their full diversity. Here we report unprecedented levels of archaeal diversity in great ape gut microbiomes, exceeding that detected by conventional 16S rRNA gene surveys. Paralleling what has been reported for bacteria, there is a vast reduction of archaeal diversity in humans. Our study demonstrates that archaeal diversity in the great ape gut microbiome greatly exceeds that reported previously and provides the basis for further studies on the role of archaea in the gut microbiome.
Highlights
Archaea are habitual residents of the human gut flora but are detected at substantially lower frequencies than bacteria
Several archaeal lineages have been maintained throughout hominoid evolution, paralleling what has been reported for bacteria, we observed a vast reduction of archaeal diversity in humans that has been accompanied by the loss of some associations between archaea and bacteria typical of other great apes
Of the 3,079,161 reads obtained with the archaeon-specific primers, 3.8% were bacterial in origin, which likely represents a low level of indiscriminate priming since the primers were designed to have complete specificity to Archaea
Summary
Archaea are habitual residents of the human gut flora but are detected at substantially lower frequencies than bacteria. Comparing microbiomes across five great ape species allowed us to examine the dynamics of archaeal lineages over evolutionary time scales These analyses revealed hundreds of gut-associated archaeal lineages, indicating that upwards of 90% of the archaeal diversity in the human and great ape gut microbiomes has been overlooked. The universal prokaryotic primers typically used to interrogate microbial communities do not fully capture the breadth of archaeal diversity [1, 7], which has potentially left vast amounts of archaeal diversity unobserved Due to these limitations, we hypothesized that the archaeal diversity within the gut microbiomes of great apes is much higher than previously recognized. Several archaeal lineages have been maintained throughout hominoid evolution, paralleling what has been reported for bacteria, we observed a vast reduction of archaeal diversity in humans that has been accompanied by the loss of some associations between archaea and bacteria typical of other great apes
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