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

Lea Sedghi1 | Vincent DiMassa2 | Anthony Harrington2 | Susan V. Lynch2 | Yvonne L. Kapila1

1 Department of Orofacial Sciences, School of Dentistry, University of California San Francisco, San Francisco, California, USA

2 Department of Medicine, University of California San Francisco, San Francisco, California, USA Correspondence Yvonne L. Kapila, Department of Orofacial Sciences, School of Dentistry, University of California San Francisco, San Francisco, CA, USA. Email: Yvonne.Kapila@ucsf.edu

1 | INTRODUCTION

The field of human microbiome research has undergone a revolution in its approach toward understanding how microorganisms influence the physiology of their host.1 Development of culture-independent methods has resulted in increased detection and classification of microbial species within microbial communities.2 technologies, biomarker sequencing, and shotgun metagenomics have become standard tools used to determine the composition and genetic makeup of the human microbiome.3 Other “-omics” technologies, such as proteomics and metabolomics, support mechanistic hypotheses involved in causal microbial pathways that are related to states of health and disease.4,5 Since Antonie van Leeuwenhoek first discovered the existence of microbes in the 1700s while analyzing dental plaque under a microscope, the composition of oral microbial communities has been extensively studied.6 Over 250 species from the oral cavity have been isolated in culture and characterized, including several key pathogens, such as Streptococcus mutans, Porphyromonas gingivalis, Tannerella forsythia, and Aggregatibacter actinomycetemcomitans, involved in the etiology of dental caries and periodontal disease.7-9 An integrated approach toward understanding states of oral disease from the polymicrobial perspective has emerged over time, attributing disease pathology not only to key pathogens but rather to networks of co-occurring microbes, the collective activities of which contribute to pathogenesis.9-12 As such, the importance of understanding the divergences, between oral health and disease, in the microbes comprising the system as well as their relative abundance and functional activity, in addition to genetic factors and ecological pressures that drive such changes, is a primary focus of research within the field of oral health research.9,13-17 In recent decades, genetic approaches have shed light on the functional capacity of members of oral microbiomes, the mechanistic underpinnings of caries and periodontal disease pathogenesis, and the complex dynamics and fitness factors of key organisms in oral microbiomes.3,18 The oral microbial ecosystem is constantly exposed to exogenous foreign substances.17 Such circumstances are defining factors for founding microbes and their ability to persist in this environment, and make for distinct relationships between microbe and host that rely on selective pressures. Pioneer microbial colonizers of the oral cavity, such as Streptococcus mitis, Streptococcus sanguinis, Streptococcus gordonii, and Streptococcus salivarius, display core characteristics that make them well suited to this specific niche as they are able to bind selectively to tongue and cheek cells before the teeth emerge and can outcompete other microbial species.17,19 Emerging teeth acquire a protective glycoprotein coat, which sets in motion successional microbial colonization, resulting in the development of complex polymicrobial biofilm communities, namely dental plaque.20 These complex dental plaque matrices create unique microenvironments that harbor acidic and anaerobic microenvironments, and thus select for organisms distinct from those growing directly on the tooth surface.

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