HIV Infection and Exposure Increases Cariogenic Taxa, Reduces Taxonomic Turnover, and Homogenizes Spatial Differentiation for the Supragingival Microbiome

Abstract

Background The oral microbiome comprises distinct microbial communities that colonize diverse ecological niches across the oral cavity, the composition of which are influenced by nutrient and substrate availability, host genetics, diet, behavior, age, and other diverse host and environmental factors. Unlike other densely populated human-associated microbial ecosystems (e.g., gut, urogenital), the oral microbiome is regularly and directly exposed to the external environment and is therefore likely less stable over time. Cross sectional studies of the oral microbiome capture a glimpse of this temporal dynamism, yet a full appreciation of the relative stability, robusticity, and spatial structure of the oral environment is necessary to understand the role of microbial communities in promoting health or disease. Results Here we investigate the spatial and temporal stability of the oral microbiome over three sampling time points in the context of HIV infection and exposure. Individual teeth were sampled from a cohort of 565 Nigerian children with varying levels of tooth decay severity (i.e., caries disease). We collected 1,960 supragingival plaque samples and characterized the oral microbiome using a metataxonomic approach targeting an approximately 478 bp region of the bacterial rpoC gene. We found that both infection and exposure to HIV have significant effects on the stability of the supragingival plaque microbiome at both the spatial and temporal scale. Specifically, we detect (1) significantly lower taxonomic turnover of the oral community among exposed and infected children compared to unexposed children, (2) we find that HIV infection homogenizes the oral community across the anterior and posterior dentition, and (3) that impaired immunity (i.e., low CD4 count) and low taxonomic turnover over time in children living with HIV is associated with higher frequency of cariogenic taxa including Streptococcus mutans. Conclusions Our results document substantial community fluctuations over time in children unexposed to HIV independent of oral health status. This suggests that the oral community, under typical conditions, rapidly adapts to environmental perturbations to maintain homeostasis and that long-term taxonomic rigidity is a signal of community dysfunction, potentially leading to a higher incidence of oral disease including caries.