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Abstract
Periodontitis is a polymicrobial, biofilm-caused, inflammatory disease affecting the tooth-supporting tissues. It is not only the leading cause of tooth loss worldwide, but can also impact systemic health. The development of effective treatment strategies is hampered by the complicated disease pathogenesis which is best described by a polymicrobial synergy and dysbiosis model. This model classifies the Gram-negative anaerobe Tannerella forsythia as a periodontal pathogen, making it a prime candidate for interference with the disease. Tannerella forsythia employs a protein O-glycosylation system that enables high-density display of nonulosonic acids via the bacterium's two-dimensional crystalline cell surface layer. Nonulosonic acids are sialic acid-like sugars which are well known for their pivotal biological roles. This review summarizes the current knowledge of T. forsythia's unique cell envelope with a focus on composition, biosynthesis and functional implications of the cell surface O-glycan. We have obtained evidence that glycobiology affects the bacterium's immunogenicity and capability to establish itself in the polymicrobial oral biofilm. Analysis of the genomes of different T. forsythia isolates revealed that complex protein O-glycosylation involving nonulosonic acids is a hallmark of pathogenic T. forsythia strains and, thus, constitutes a valuable target for the design of novel anti-infective strategies to combat periodontitis.
Highlights
To proliferate and persist in the oral cavity, bacteria tend to live in biofilms which are clinically described as oral plaque
Nonulosonic acids are sialic acid-like sugars which are well known for their pivotal biological roles
In contrast to the scarcity of evidence for their function, an increasing number of studies suggest that pseudaminic acid (Pse) and legionaminic acid (Leg) derivatives are widespread among prokaryotes, where more than 20% of 1000 microbial genomes examined were found to encode a predicted Nonulosonic acids (NulOs) biosynthesis pathway [45]
Summary
To proliferate and persist in the oral cavity, bacteria tend to live in biofilms which are clinically described as oral plaque. Oral bacteria exist in a natural balance with the host Different factors such as smoking, diabetes, genetic predisposition or poor dental hygiene can cause the community to become dysbiotic, enabling potentially pathogenic bacteria to increase in numbers and cause persistent infections, such as periodontitis. A number of potential pathogens promoting the onset of the disease have been identified through highthroughput sequencing, and metagenomic, metatranscriptomic as well as mechanistic studies [11,12,13] These include the pathogens Tannerella forsythia, Porphyromonas gingivalis and Treponema denticola constituting the so-called ‘red complex’, a group of bacteria clearly associated with periodontal disease and classified as highly virulent [3,9,10,14]. We and others have obtained evidence that a complex, protein-bound O-glycan which is displayed at high density on the bacterial cell surface [20] underpins the pathogenicity of T. forsythia [21,22,23,24]
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