The Bifidobacterium dentium Bd1 Genome Sequence Reflects Its Genetic Adaptation to the Human Oral Cavity

Marco Ventura,Maria Mantzourani,Gerald F Fitzgerald,Beile Gao,Marcus J Claesson,Fei He,Laura Mulas,Francesca Bottacini,Alberto Ferrarini,David Beighton,Radhey S Gupta,Francesca Turroni,Massimo Delledonne,Douwe Van Sinderen,Vanessa Giubellini,Aldert Zomer,Carlos Canchaya,Bernard Henrissat,Ziding Zhang,Elena Foroni,Paul W O’toole ,Marco R Oggioni ,Pedro M Coutinho

doi:10.1371/journal.pgen.1000785

Abstract

Bifidobacteria, one of the relatively dominant components of the human intestinal microbiota, are considered one of the key groups of beneficial intestinal bacteria (probiotic bacteria). However, in addition to health-promoting taxa, the genus Bifidobacterium also includes Bifidobacterium dentium, an opportunistic cariogenic pathogen. The genetic basis for the ability of B. dentium to survive in the oral cavity and contribute to caries development is not understood. The genome of B. dentium Bd1, a strain isolated from dental caries, was sequenced to completion to uncover a single circular 2,636,368 base pair chromosome with 2,143 predicted open reading frames. Annotation of the genome sequence revealed multiple ways in which B. dentium has adapted to the oral environment through specialized nutrient acquisition, defences against antimicrobials, and gene products that increase fitness and competitiveness within the oral niche. B. dentium Bd1 was shown to metabolize a wide variety of carbohydrates, consistent with genome-based predictions, while colonization and persistence factors implicated in tissue adhesion, acid tolerance, and the metabolism of human saliva-derived compounds were also identified. Global transcriptome analysis demonstrated that many of the genes encoding these predicted traits are highly expressed under relevant physiological conditions. This is the first report to identify, through various genomic approaches, specific genetic adaptations of a Bifidobacterium taxon, Bifidobacterium dentium Bd1, to a lifestyle as a cariogenic microorganism in the oral cavity. In silico analysis and comparative genomic hybridization experiments clearly reveal a high level of genome conservation among various B. dentium strains. The data indicate that the genome of this opportunistic cariogen has evolved through a very limited number of horizontal gene acquisition events, highlighting the narrow boundaries that separate commensals from opportunistic pathogens.

Highlights

Bifidobacteria are relatively abundant inhabitants of the gastrointestinal tract (GIT) of humans and animals [1]
Bifidobacteria have been isolated from the human oral cavity, where their presence is linked to the progression of tooth decay: bifidobacteria have been detected in high numbers in infected dentine from carious lesions in children [9] and have been associated with childhood dental caries [10]
In recent surveys of oral bifidobacteria associated with coronal caries in adults and children [17] and root caries in adults [18], B. dentium was the most frequently isolated Bifidobacterium species, representing approximately eight percent of the culturable bacteria isolated from active carious lesions

Summary

Introduction

Bifidobacteria are relatively abundant inhabitants of the gastrointestinal tract (GIT) of humans and animals [1]. In recent surveys of oral bifidobacteria associated with coronal caries in adults and children [17] and root caries in adults [18], B. dentium was the most frequently isolated Bifidobacterium species, representing approximately eight percent of the culturable bacteria isolated from active carious lesions. This species is capable of acidogenesis to produce a final pH in glucose-containing media

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Discussion

Conclusion