Fusobacterium nucleatum and Tannerella forsythia Induce Synergistic Alveolar Bone Loss in a Mouse Periodontitis Model

Settem, Rajendra P.; Elhassan, Ahmed; Honma, Kiyonobu; Stafford, Graham P.; Sharma, Ashu

doi:10.1128/iai.06276-11

Cited by 90 publications

(76 citation statements)

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“…1a). Several other bacteria have also been implicated, including but not limited to Tannerella forsythia, Aggregatibacter actinomycetemcomitans, and Fusobacterium nucleatum [31,32]. Given the diversity and numbers of other bacteria in and around the periodontal neighbourhood, then it is difficult to say with absolute certainty that particular periodontal pathogens are the sole cause of periodontitis.…”

Section: Periodontal Disease: An Uncontrolled Ganglandmentioning

confidence: 99%

Fungi at the Scene of the Crime: Innocent Bystanders or Accomplices in Oral Infections?

Delaney

Kean

Short

et al. 2018

Curr Clin Micro Rpt

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Purpose of Review Over the last decade, microbiome studies have enhanced our knowledge and understanding of the polymicrobial nature of oral infections. Recently, profiling of the fungal microbiome has expanded our conventional understanding of oral ecology, revealing the critical importance of yeasts within this complex microbiome. This review aims to explore our current appreciation of interkingdom interactions in oral disease. Recent Findings There is a growing evidence base of interactions and pathogenic synergy and antagonism with bacterial species within oral disease. Recent studies have helped to develop our knowledge of how Candida albicans, alongside bacteria such as Porphyromonas gingivalis, Streptococcus mutans, Staphylococcus aureus, Enterococcus faecalis, and Lactobacillus species, influence overall pathogenicity. Summary Clinical and experimental evidence makes a compelling case for a role for C. albicans in a number of oral infections, though whether its role is an active accomplice or passive bystander remains to be determined.

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Section: Periodontal Disease: An Uncontrolled Ganglandmentioning

confidence: 99%

Fungi at the Scene of the Crime: Innocent Bystanders or Accomplices in Oral Infections?

Delaney

Kean

Short

et al. 2018

Curr Clin Micro Rpt

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Section: Oral Infectionmentioning

confidence: 99%

“…The resulting infected area was swabbed for PCR analysis, and maxillae and mandibles were retrieved for alveolar bone resorption analysis [90]. T. forsythia and F. nucleatum caused more severe alveolar bone loss than other combinations of microbes tested, which the investigators had predicted due to their synergistic ability to form larger biofilms in vitro [91].A rat pup model was used to demonstrate a synergistic interaction between Streptococcus mutans and C. albicans during oral infection [92]. Pups were first screened and cleared of any endogenous S. mutans and C. albicans colonization, then infected with S. mutans for 23 days, followed by C. albicans for an additional 2 weeks.…”

mentioning

confidence: 99%

“…Plaque biofilms were then harvested, sonicated and plated for growth, and the teeth were analyzed for the progression of dental caries [92]. Coinfected pups had larger biofilms and more virulent infections, which more severely eroded their enamel than did pups given monospecies infections.As microbes present in the normal oral flora can complicate the interpretation of polymicrobial interactions, antibiotics and mouth rinses are frequently used to clear the native oral flora prior to inoculating [90,91]; alternatively, a murine abscess model has been utilized to study interactions between oral microbes, in the absence of the oral flora [29]. Utilizing a murine thigh abscess model, Ramsey et al co-cultured the oral commensal species Streptococcus gordonii and the opportunistic oral pathogen A. actinomycetemcomitans, and demonstrated that metabolite cross-feeding between the two species correlated with virulence.…”

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confidence: 99%

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Biofilm Models of Polymicrobial Infection

2015

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Interactions between microbes are complex and play an important role in the pathogenesis of infections. These interactions can range from fierce competition for nutrients and niches to highly evolved cooperative mechanisms between different species that support their mutual growth. An increasing appreciation for these interactions, and desire to uncover the mechanisms that govern them, has resulted in a shift from monomicrobial to polymicrobial biofilm studies in different disease models. Here we provide an overview of biofilm models used to study select polymicrobial infections and highlight the impact that the interactions between microbes within these biofilms have on disease progression. Notable recent advances in the development of polymicrobial biofilm-associated infection models and challenges facing the study of polymicrobial biofilms are addressed. Polymicrobial interactions in biofilmsOver the past 2 decades there has been a revolutionary paradigm shift in the field of microbiology with the appreciation that bacteria present in most biological systems exist in biofilms, rather than in a free-living state. This understanding has dramatically changed the way we study bacteria in the laboratory and resulted in the development of many new experimental systems that replicate biofilm environments [1][2][3][4][5]. Studies utilizing these systems have demonstrated time and time again that bacteria behave very differently when in a biofilm than during planktonic growth. In many ways, we now have to relearn everything we thought we knew about bacterial behavior through the view of the biofilm lens.Similarly, the recent explosion of metagenomic studies has significantly increased our appreciation of the complexity of the microbial populations present in biofilms [6,7]. This is also true for infections, most of which are thought to be biofilm related and inherently polymicrobial, including various species of bacteria, fungi and viruses [8]. It is thought that microbes act in concert to establish biofilms, which in turn can increase tolerance to antimicrobials, exacerbate of the host's immune response and increase persistence at the infection site [7,[9][10][11].Genetic diversity of microbes within biofilm communities is thought to increase the fitness of the residing community, making them more equipped to survive environmental stresses. In large part, this is due to an expanded gene pool, which can be more easily shared within the confines of a biofilm community [12]. Community composition and interactions within the community can have huge influences on bacterial behavior. Thus, just as the behavior of planktonic versus biofilm-associated bacteria is dramatically different, so is that of bacteria in single species versus multispecies systems.Interactions between microbes are complex and highly dependent on context. They can range from fierce competition for nutrients and niches, manifested by antagonistic behavior, to highly evolved cooperative mechanisms between different species that support their mutual grow...

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“…forsythia, a common pathogen present in dental biofilms, is implicated in periodontitis. Its role in the disease process has been confirmed in animal models (1), and it has been demonstrated that the bacterium's ability to induce disease is enhanced when coinfected with other bacteria such as Fusobacterium nucleatum (22). Strikingly, T. forsythia depends on exogenous MurNAc, an essential peptidoglycan amino sugar, for growth.…”

Section: Discussionmentioning

confidence: 83%

Identification of a Novel N -Acetylmuramic Acid Transporter in Tannerella forsythia

et al. 2016

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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 PTSindependent 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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Fusobacterium nucleatum and Tannerella forsythia Induce Synergistic Alveolar Bone Loss in a Mouse Periodontitis Model

Abstract: ABSTRACTTannerella forsythiais strongly associated with chronic periodontitis, an inflammatory disease of the tooth-supporting tissues, leading to tooth loss.Fusobacterium nucleatum, an opportunistic pathogen, is tho… Show more

Cited by 90 publications

References 50 publications

Fungi at the Scene of the Crime: Innocent Bystanders or Accomplices in Oral Infections?

Fungi at the Scene of the Crime: Innocent Bystanders or Accomplices in Oral Infections?

Biofilm Models of Polymicrobial Infection

Identification of a Novel N -Acetylmuramic Acid Transporter in Tannerella forsythia

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