Abstract

Humans are host to a multitude of microorganisms that rapidly populate the body at birth, subject to a complex interplay that is dependent on host genetics, lifestyle, and environment. The host-associated microbiome, including the oral microbiome, presents itself in a complex ecosystem important to health and disease. As the most common chronic disease globally, dental caries is induced by host-microbial dysbiosis in children and adults. Multiple biological and environmental factors are likely to impact disease predisposition, onset, progression, and severity, yet longitudinal studies able to capture these influences are missing. To investigate how host genetics and environment influenced the oral microbial communities over time, we profiled supragingival plaque microbiomes of dizygotic and monozygotic twins during 3 visits over 12-months. Dental plaque DNA samples were amplified by targeting the 16S rRNA gene V4 region, and microbial findings were correlated with clinical, diet and genetic metadata. We observed that the oral microbiome variances were shaped primarily by the environment when compared to host genetics. Among the environmental factors shaping microbial changes of our subjects, significant metadata included age of the subject, and the age by which subjects initiated brushing habits, and the types of actions post-brushing. Relevant heritability of the microbiome included Actinomyces and Capnocytophaga in monozygotic twins and Kingella in dizygotic twins. Corynebacterium and Veillonella abundances were associated with age, whereas Aggregatibacter was associated with younger subjects. Streptococcus abundance showed an inverse association over time, and Selenomonas abundances increased with brushing frequency per day. Unraveling the exact biological mechanisms in caries has the potential to reveal novel host-microbial biomarkers, pathways, and targets important to effective preventive measures, and early disease control in children.

Highlights

  • Across various human body habitats, including the oral cavity, mutually beneficial relationships between the host and its microbiome lead to homeostatic phenotypic patterns

  • In an earlier cross-sectional investigation by our group, we investigated the relationship between the oral microbiome, host-associated microbial communities, host genetics, and environmental factors in the caries phenotypes in 485 dizygotic and monozygotic twins (241 twin pairs and one set of triplets) aged 5–11 at a single visit[10,11]

  • Microbial dissimilarity was estimated by Bray–Curtis index, and the results showed that differences initially influenced by inherited genetic backgrounds reduced over time from visit 1 to visit 3 (Fig. 1)

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Summary

Introduction

Across various human body habitats, including the oral cavity, mutually beneficial relationships between the host and its microbiome lead to homeostatic phenotypic patterns. Loss of host-microbial homeostasis in the oral habitat leads to dysbiosis and a range of oral and systemic conditions, including caries, periodontal disease, and cancers. In an earlier cross-sectional investigation by our group, we investigated the relationship between the oral microbiome, host-associated microbial communities, host genetics, and environmental factors in the caries phenotypes in 485 dizygotic and monozygotic twins (241 twin pairs and one set of triplets) aged 5–11 at a single visit[10,11]. We have evaluated the extent that caries had advanced through the enamel and penetrated into the dentin or just remained confined within the enamel clinically In this longitudinal analysis, we evaluated the supragingival microbiome found in plaque (biofilm) from twin pairs with or without carious lesions. We observed that the most heritable taxa were associated with the subject brushing habits and age

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