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Sialic acid, periodontal pathogens and Tannerella forsythia: stick around and enjoy the feast!

ABSTRACT: Periodontal pathogens, like any other human commensal or pathogenic bacterium, must possess both the ability to acquire the necessary growth factors and the means to adhere to surfaces or reside and survive in their environmental niche. Recent evidence has suggested that sialic acid containing host molecules may provide both of these requirements in vivo for several periodontal pathogens but most notably for the red complex organism Tannerella forsythia. Several other periodontal pathogens also possess sialic acid scavenging enzymes - sialidases, which can also expose adhesive epitopes, but might also act as adhesins in their own right. In addition, recent experimental work coupled with the release of several genome sequences has revealed that periodontal bacteria have a range of sialic acid uptake and utilization systems while others may also use sialic acid as a cloaking device on their surface to mimic host and avoid immune recognition. This review will focus on these systems in a range of periodontal bacteria with a focus on Ta. forsythia.

SUBMITTER: Stafford G

PROVIDER: S-EPMC4049603 | biostudies-literature | 2012 Feb

REPOSITORIES: biostudies-literature

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Sialic acid, periodontal pathogens and Tannerella forsythia: stick around and enjoy the feast!

Stafford G G Roy S S Honma K K Sharma A A

Molecular oral microbiology 20111112 1

Periodontal pathogens, like any other human commensal or pathogenic bacterium, must possess both the ability to acquire the necessary growth factors and the means to adhere to surfaces or reside and survive in their environmental niche. Recent evidence has suggested that sialic acid containing host molecules may provide both of these requirements in vivo for several periodontal pathogens but most notably for the red complex organism Tannerella forsythia. Several other periodontal pathogens also ...[more]

PMID: 22230462

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Project description:BACKGROUND:Tannerella forsythia is a bacterial pathogen implicated in periodontal disease. Numerous virulence-associated T. forsythia genes have been described, however, it is necessary to expand the knowledge on T. forsythia's genome structure and genetic repertoire to further elucidate its role within pathogenesis. Tannerella sp. BU063, a putative periodontal health-associated sister taxon and closest known relative to T. forsythia is available for comparative analyses. In the past, strain confusion involving the T. forsythia reference type strain ATCC 43037 led to discrepancies between results obtained from in silico analyses and wet-lab experimentation. RESULTS:We generated a substantially improved genome assembly of T. forsythia ATCC 43037 covering 99% of the genome in three sequences. Using annotated genomes of ten Tannerella strains we established a soft core genome encompassing 2108 genes, based on orthologs present in >?=?80% of the strains analysed. We used a set of known and hypothetical virulence factors for comparisons in pathogenic strains and the putative periodontal health-associated isolate Tannerella sp. BU063 to identify candidate genes promoting T. forsythia's pathogenesis. Searching for pathogenicity islands we detected 38 candidate regions in the T. forsythia genome. Only four of these regions corresponded to previously described pathogenicity islands. While the general protein O-glycosylation gene cluster of T. forsythia ATCC 43037 has been described previously, genes required for the initiation of glycan synthesis are yet to be discovered. We found six putative glycosylation loci which were only partially conserved in other bacteria. Lastly, we performed a comparative analysis of translational bias in T. forsythia and Tannerella sp. BU063 and detected highly biased genes. CONCLUSIONS:We provide resources and important information on the genomes of Tannerella strains. Comparative analyses enabled us to assess the suitability of T. forsythia virulence factors as therapeutic targets and to suggest novel putative virulence factors. Further, we report on gene loci that should be addressed in the context of elucidating T. forsythia's protein O-glycosylation pathway. In summary, our work paves the way for further molecular dissection of T. forsythia biology in general and virulence of this species in particular.

Project description:Tannerella forsythia is a Gram-negative periodontal pathogen lacking the ability to undergo de novo synthesis of amino sugars N-acetylmuramic acid (MurNAc) and N-acetylglucosamine (GlcNAc) that form the disaccharide repeating unit of the peptidoglycan backbone. T. forsythia relies on the uptake of these sugars from the environment, which is so far unexplored. Here, we identified a novel transporter system of T. forsythia involved in the uptake of MurNAc across the inner membrane and characterized a homolog of the Escherichia coli MurQ etherase involved in the conversion of MurNAc-6-phosphate (MurNAc-6-P) to GlcNAc-6-P. The genes encoding these components were identified on a three-gene cluster spanning Tanf_08375 to Tanf_08385 located downstream from a putative peptidoglycan recycling locus. We show that the three genes, Tanf_08375, Tanf_08380, and Tanf_08385, encoding a MurNAc transporter, a putative sugar kinase, and a MurQ etherase, respectively, are transcriptionally linked. Complementation of the Tanf_08375 and Tanf_08380 genes together in trans, but not individually, rescued the inability of an E. coli mutant deficient in the phosphotransferase (PTS) system-dependent MurNAc transporter MurP as well as that of a double mutant deficient in MurP and components of the PTS system to grow on MurNAc. In addition, complementation with this two-gene construct in E. coli caused depletion of MurNAc in the medium, further confirming this observation. Our results show that the products of Tanf_08375 and Tanf_08380 constitute a novel non-PTS MurNAc transporter system that seems to be widespread among bacteria of the Bacteroidetes phylum. To the best of our knowledge, this is the first identification of a PTS-independent MurNAc transporter in bacteria.ImportanceIn this study, we report the identification of a novel transporter for peptidoglycan amino sugar N-acetylmuramic acid (MurNAc) in the periodontal pathogen T. forsythia It has been known since the late 1980s that T. forsythia is a MurNAc auxotroph relying on environmental sources for this essential sugar. Most sugar transporters, and the MurNAc transporter MurP in particular, require a PTS phosphorelay to drive the uptake and concurrent phosphorylation of the sugar through the inner membrane in Gram-negative bacteria. Our study uncovered a novel type of PTS-independent MurNAc transporter, and although so far, it seems to be unique to T. forsythia, it may be present in a range of bacteria both of the oral cavity and gut, especially of the phylum Bacteroidetes.

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Sialic acid, periodontal pathogens and Tannerella forsythia: stick around and enjoy the feast!

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Sialic acid, periodontal pathogens and Tannerella forsythia: stick around and enjoy the feast!

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