Characterizing the evolution of the oral microbiome is a challenging, but increasingly feasible, task. Recently, dental calculus has been shown to preserve ancient biomolecules from the oral microbiota, host tissues and diet for tens of thousands of years. As such, it provides a unique window into the ancestral oral microbiome. This article reviews recent advancements in ancient dental calculus research and emerging insights into the evolution and ecology of the human oral microbiome.
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Functional diversity of microbial ecologies estimated from ancient human coprolites and dental calculus
Human microbiome studies are increasingly incorporating macroecological approaches, such as community assembly, network analysis and functional redundancy to more fully characterize the microbiome. Such analyses have not been applied to ancient human microbiomes, preventing insights into human microbiome evolution. We address this issue by analysing published ancient microbiome datasets: coprolites from Rio Zape ( n = 7; 700 CE Mexico) and historic dental calculus ( n = 44; 1770–1855 CE, UK), as well as two novel dental calculus datasets: Maya ( n = 7; 170 BCE-885 CE, Belize) and Nuragic Sardinians ( n = 11; 1400–850 BCE, Italy). Periodontitis-associated bacteria ( Treponema denticola , Fusobacterium nucleatum and Eubacterium saphenum ) were identified as keystone taxa in the dental calculus datasets. Coprolite keystone taxa included known short-chain fatty acid producers ( Eubacterium biforme, Phascolarctobacterium succinatutens ) and potentially disease-associated bacteria ( Escherichia , Brachyspira) . Overlap in ecological profiles between ancient and modern microbiomes was indicated by similarity in functional response diversity profiles between contemporary hunter–gatherers and ancient coprolites, as well as parallels between ancient Maya, historic UK, and modern Spanish dental calculus; however, the ancient Nuragic dental calculus shows a distinct ecological structure. We detected key ecological signatures from ancient microbiome data, paving the way to expand understanding of human microbiome evolution. This article is part of the theme issue ‘Insights into health and disease from ancient biomolecules’.
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- Award ID(s):
- 1925579
- PAR ID:
- 10232929
- Date Published:
- Journal Name:
- Philosophical Transactions of the Royal Society B: Biological Sciences
- Volume:
- 375
- Issue:
- 1812
- ISSN:
- 0962-8436
- Page Range / eLocation ID:
- 20190586
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Objectives This study examines biological indicators of dental disease and nonspecific stress in human remains of three high altitude Himalayan archaeological sites to test whether shared ecological constraints led to similar bioarchaeological profiles in these markers.
Methods Samples (
n = 170) derive from three sites in Nepal dating to two periods (400–50 BCE and c. 400–650 CE). Dental diseases (caries, antemortem tooth loss, and abscesses) were assessed by both the number of individuals and the number of elements observed, while childhood stress markers included observation of growth disruptions (enamel hypoplasia and adult femur length/stature) and cranial porosities. Statistical analysis included chi‐square and Fisher's exact tests for categorical data and ANOVA and t‐tests for metric data.Results There are significant differences between the sites and sexes in frequencies of dental diseases in the adult samples. There are low frequencies of childhood stress markers overall and the femur length data show no significant differences across sites, but significant sexual dimorphism within each site. Females have reduced stature compared to contemporary Tibetan samples residing at a similar elevation.
Conclusions Variations in dental disease frequencies between the sites may be due to local variations in microenvironment, cultural, and/or temporal differences in resource availability, food consumption and preparation, as well as the age structure of the samples. The low frequencies of markers for nonspecific stress may be indicative of the ability of these ancient Himalayan groups to successfully meet the challenges posed by the extreme conditions of high altitude living through biocultural adaptations.
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ABSTRACT Small molecules are the primary communication media of the microbial world. Recent bioinformatic studies, exploring the biosynthetic gene clusters (BGCs) which produce many small molecules, have highlighted the incredible biochemical potential of the signaling molecules encoded by the human microbiome. Thus far, most research efforts have focused on understanding the social language of the gut microbiome, leaving crucial signaling molecules produced by oral bacteria and their connection to health versus disease in need of investigation. In this study, a total of 4,915 BGCs were identified across 461 genomes representing a broad taxonomic diversity of oral bacteria. Sequence similarity networking provided a putative product class for more than 100 unclassified novel BGCs. The newly identified BGCs were cross-referenced against 254 metagenomes and metatranscriptomes derived from individuals either with good oral health or with dental caries or periodontitis. This analysis revealed 2,473 BGCs, which were differentially represented across the oral microbiomes associated with health versus disease. Coabundance network analysis identified numerous inverse correlations between BGCs and specific oral taxa. These correlations were present in healthy individuals but greatly reduced in individuals with dental caries, which may suggest a defect in colonization resistance. Finally, corroborating mass spectrometry identified several compounds with homology to products of the predicted BGC classes. Together, these findings greatly expand the number of known biosynthetic pathways present in the oral microbiome and provide an atlas for experimental characterization of these abundant, yet poorly understood, molecules and socio-chemical relationships, which impact the development of caries and periodontitis, two of the world’s most common chronic diseases. IMPORTANCE The healthy oral microbiome is symbiotic with the human host, importantly providing colonization resistance against potential pathogens. Dental caries and periodontitis are two of the world’s most common and costly chronic infectious diseases and are caused by a localized dysbiosis of the oral microbiome. Bacterially produced small molecules, often encoded by BGCs, are the primary communication media of bacterial communities and play a crucial, yet largely unknown, role in the transition from health to dysbiosis. This study provides a comprehensive mapping of the BGC repertoire of the human oral microbiome and identifies major differences in health compared to disease. Furthermore, BGC representation and expression is linked to the abundance of particular oral bacterial taxa in health versus dental caries and periodontitis. Overall, this study provides a significant insight into the chemical communication network of the healthy oral microbiome and how it devolves in the case of two prominent diseases.more » « less
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Abstract Objectives Dental calculus is among the richest known sources of ancient DNA in the archaeological record. Although most DNA within calculus is microbial, it has been shown to contain sufficient human DNA for the targeted retrieval of whole mitochondrial genomes. Here, we explore whether calculus is also a viable substrate for whole human genome recovery using targeted enrichment techniques.
Materials and methods Total DNA extracted from 24 paired archaeological human dentin and calculus samples was subjected to whole human genome enrichment using in‐solution hybridization capture and high‐throughput sequencing.
Results Total DNA from calculus exceeded that of dentin in all cases, and although the proportion of human DNA was generally lower in calculus, the absolute human DNA content of calculus and dentin was not significantly different. Whole genome enrichment resulted in up to four‐fold enrichment of the human endogenous DNA content for both dentin and dental calculus libraries, albeit with some loss in complexity. Recovering more on‐target reads for the same sequencing effort generally improved the quality of downstream analyses, such as sex and ancestry estimation. For nonhuman DNA, comparison of phylum‐level microbial community structure revealed few differences between precapture and postcapture libraries, indicating that off‐target sequences in human genome‐enriched calculus libraries may still be useful for oral microbiome reconstruction.
Discussion While ancient human dental calculus does contain endogenous human DNA sequences, their relative proportion is low when compared with other skeletal tissues. Whole genome enrichment can help increase the proportion of recovered human reads, but in this instance enrichment efficiency was relatively low when compared with other forms of capture. We conclude that further optimization is necessary before the method can be routinely applied to archaeological samples.
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- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rstb.2019.0586
