Sequencing ancient calcified dental plaque shows changes in oral microbiota with dietary shifts of the Neolithic and Industrial revolutions

Abstract

The importance of commensal microbes for human health is increasingly recognized [1][2][3][4][5] , yet the impacts of evolutionary changes in human diet and culture on commensal microbiota remain almost unknown. Two of the greatest dietary shifts in human evolution involved the adoption of carbohydrate-rich Neolithic (farming) diets 6,7 (beginning ~10,000 years BP 6,8 ), and the more recent advent of industrially processed flour and sugar (~1850) 9 . Here, we show that calcified dental plaque (dental calculus) on ancient teeth preserves a detailed genetic record throughout this period. Data from 34 early European skeletons indicate that the transition from hunter-gatherer to farming shifted the oral microbial community to a disease-associated configuration. The composition of oral microbiota remained surprisingly constant between Neolithic and Medieval times, after which (the now ubiquitous) cariogenic bacteria became dominant, apparently during the Industrial Revolution. Modern oral microbiota are markedly less diverse than historic Sequence data have been deposited in Genbank under accession ERP002107.The authors declare no competing financial interests. Europe PMC Funders GroupAuthor Manuscript Nat Genet. Author manuscript; available in PMC 2014 April 23. Commensal microbiota comprise the majority of cells in the body and play a key role in human health [1][2][3][4][5]10 . However, their evolution remains poorly understood, and detailed genetic records from commensal bacteria have yet to be recovered from the archaeological record. Dental calculus is ubiquitous in both present-day and ancient human populations 11 , and microscopic analysis has shown that it accurately preserves bacterial morphology over millennia [12][13][14] . Dental calculus develops when dental plaque, an extremely dense bacterial biofilm 15 , becomes mineralised with calcium phosphate 16 . Bacteria in calculus become locked in a crystalline matrix similar to bone 16 (Supplementary Figure 1), with deposits occurring both above and below the gum or gingiva (supra-and subgingivally) 17 . Calculus represents one of the few sources of preserved human and hominid microbiota, and genetic analysis has the potential to create a powerful new record of past dietary impacts, health changes, and oral pathogen genomic evolution deep into the past. In addition, oral bacteria are transferred vertically from the primary caregiver(s) in early childhood 18 and horizontally between family members later in life 18,19 , making archaeological dental calculus a potentially unique means of tracing population structure, movement and admixture between ancient cultures, as well as the spread of diseases.The increased consumption of domesticated cereals (wheat and barley in the Near East) beginning with the Neolithic was associated with a marked increase in prevalence of dental calculus and oral pathology 20 . These oral diseases include dental caries (tooth decay) 1 and periodontal disease (an infection causing damage to the supporting connective tissues of ...

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