The oral microbiome: Role of key organisms and complex networks in oral health and disease

Abstract

States of oral health and disease reflect the compositional and functional capacities of, as well as the interspecies interactions within, the oral microbiota. The oral cavity exists as a highly dynamic microbial environment that harbors many distinct substrata and microenvironments that house diverse microbial communities. Specific to the oral cavity, the nonshedding dental surfaces facilitate the development of highly complex polymicrobial biofilm communities, characterized not only by the distinct microbes comprising them, but cumulatively by their activities. Adding to this complexity, the oral cavity faces near-constant environmental challenges, including those from host diet, salivary flow, masticatory forces, and introduction of exogenous microbes. The composition of the oral microbiome is shaped throughout life by factors including host genetics, maternal transmission, as well as environmental factors, such as dietary habits, oral hygiene practice, medications, and systemic factors. This dynamic ecosystem presents opportunities for oral microbial dysbiosis and the development of dental and periodontal diseases. The application of both in vitro and culture-independent approaches has broadened the mechanistic understandings of complex polymicrobial communities within the oral cavity, as well as the environmental, local, and systemic underpinnings that influence the dynamics of the oral microbiome. Here, we review the present knowledge and current understanding of microbial communities within the oral cavity and the influences and challenges upon this system that encourage homeostasis or provoke microbiome perturbation, and thus contribute to states of oral health or disease.

FIGURE 1

The Oral Microbiome: From First Encounters to Lifelong Encounters. Prenatal. The prenatal oral cavity is thought to be sterile until birth, with colonization occurring soon after delivery. The composition of the oral microbiota in infants has been shown to correlate with mode of delivery. However, infants share an oral microbiota similar to that of their mothers, suggesting that the infant oral microbiota may derive from hematogenous or intrauterine transmission from the mother. Detection of oral microbes of maternal origin among several intrauterine locations, as well as associations with adverse pregnancy outcomes, demonstrate the role of the maternal oral microbiome in prenatal health and suggests in utero colonization. Early life. Microbial colonization begins shortly following birth through vertical transmission from the mother, transmission from the diet, and transmission from infant‐to‐human interactions. Microbial diversity increases upon eruption of primary teeth as this process permits the expansion of microbial niches in the oral cavity. Eruption of primary teeth also results in deviation from the maternal oral microbiota. As children age, their oral microbiotas begin to stabilize. Adult life. The oral microbiota continues to be shaped throughout life by genetic and environmental factors. Environmental factors that influence the composition and function of the oral microbiome include diet, stress, oral hygiene practices, drinking alcohol, and smoking. Genetic factors are linked to conserved phylogenetic and functional microbial signatures related to development of dental caries and heritable predisposition to periodontal disease. Aging and systemic disease. Oral microbiome diversity has been shown to decrease with age. The phylogeny and functional signatures of the oral microbiome are linked to states of dental and periodontal diseases, as well as being implicated in various systemic diseases, including cardiovascular disease, cancers, and Alzheimer's disease. Systemic conditions, such as stress and diabetes, can additionally affect the oral microbiome. Figure courtesy of Dr Ryutaro Kuraji, Assistant Professor, Department of Life Science Dentistry, The Nippon Dental University, Tokyo, Japan; Department of Periodontology, The Nippon Dental University School of Life Dentistry at Tokyo, Tokyo, Japan; Visiting Assistant Professor, Department of Orofacial Sciences, School of Dentistry, University of California San Francisco, San Francisco, CA, USA