Abstract
Loss of gut microbial diversity1–6 in industrial populations is associated with chronic diseases7, underscoring the importance of studying our ancestral gut microbiome. However, relatively little is known about the composition of pre-industrial gut microbiomes. Here we performed a large-scale de novo assembly of microbial genomes from palaeofaeces. From eight authenticated human palaeofaeces samples (1,000–2,000 years old) with well-preserved DNA from southwestern USA and Mexico, we reconstructed 498 medium- and high-quality microbial genomes. Among the 181 genomes with the strongest evidence of being ancient and of human gut origin, 39% represent previously undescribed species-level genome bins. Tip dating suggests an approximate diversification timeline for the key human symbiont Methanobrevibacter smithii. In comparison to 789 present-day human gut microbiome samples from eight countries, the palaeofaeces samples are more similar to non-industrialized than industrialized human gut microbiomes. Functional profiling of the palaeofaeces samples reveals a markedly lower abundance of antibiotic-resistance and mucin-degrading genes, as well as enrichment of mobile genetic elements relative to industrial gut microbiomes. This study facilitates the discovery and characterization of previously undescribed gut microorganisms from ancient microbiomes and the investigation of the evolutionary history of the human gut microbiota through genome reconstruction from palaeofaeces.
Highlights
Reconstruction of metagenome-assembled genomes (MAGs) is an emerging approach to recover high-quality genomes and previously undescribed species-level genome bins (SGBs) from shotgun metagenomics data
Despite the potential of de novo assembly to discover previously undescribed SGBs, this method has not been applied to palaeofaeces because of the challenges posed by highly damaged DNA
Using simulated short-read sequencing data, we show that ancient DNA damage does not significantly affect the simulated assembled genomes (Extended Data Fig. 9 and Supplementary Information section 6)
Summary
It is not known to what extent the human microbiome has evolved over long time spans. 2b, 3), shedding light on the evolutionary relationships between the ancient genomes and their modern relatives These analyses were possible due to the extraordinary preservation of the palaeofaeces, use of aDNA extraction methods suited for palaeofaeces[33], high sequencing depth (100,000,000–400,000,000 read pairs per sample) and advances in de novo genome reconstruction methodology[13]. Microbotanical analysis reveals that most of the palaeofaeces from Boomerang Shelter were deposited in the spring, summer or autumn, except for UT30.3, which was deposited in late autumn or early winter (Supplementary Table 2) This is the ideal environment for preservation owing to lack of decomposers[37] and might explain the low damage levels of UT30.3. We establish that palaeofaeces with well-preserved DNA are abundant sources of microbial genomes, including previously undescribed microbial species, that may elucidate the evolutionary histories of human microbiomes. C. New insights from uncultivated genomes of the global human gut microbiome. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
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