Abstract

The classic organization by Socransky and coworkers categorized the oral bacteria of the subgingival plaque into different complexes. Treponema denticola, Porphyromonas gingivalis and Tannerella forsythia are grouped into the red complex that is highly correlated with periodontal disease. Socransky's work closely associates red with orange complex species such as Fusobacterium nucleatum and Prevotella intermedia but not with members of the other complexes. While the relationship between species contained by these complexes is in part supported by their ability to physically attach to each other, the physiological consequences of these interactions and associations are less clear. In this study, we employed T. denticola as a model organism to analyze contact-dependent responses to interactions with species belonging to the same complex (P. gingivalis and T. forsythia), the closely associated orange complex (using F. nucleatum and P. intermedia as representatives) and the unconnected yellow complex (using Streptococcus sanguinis and S. gordonii as representatives). RNA was extracted from T. denticola alone as well as after pairwise co-incubation for 5 hrs with representatives of the different complexes, and the respective gene expression profiles were determined using microarrays. Numerous genes related to motility, metabolism, transport, outer membrane and hypothetical proteins were differentially regulated in T. denticola in the presence of the tested partner species. Further analysis revealed a significant overlap in the affected genes and we identified a general response to the presence of other species, those specific to two of the three complexes as well as individual complexes. Most interestingly, many predicted major antigens (e.g. flagella, Msp, CTLP) were suppressed in responses that included red complex species indicating that the presence of the most closely associated species induces immune-evasive strategies. In summary, the data presented here provide an in-depth understanding of the transcriptional responses triggered by contact-dependent interactions between microorganisms inhabiting the periodontal pocket.

Highlights

  • T. denticola is considered to be a significant contributor to periodontal disease and its abundance is highly correlated with periodontal pocket depth, an important indicator of disease severity [1,2,3]

  • Advances have been made in understanding signaling events in T. denticola triggered by environmental conditions associated with periodontal disease [5,6,7], the molecular mechanisms associated with its response to other oral bacterial species are largely unknown

  • ATCC 23726, Streptococcus sanguinis ATCC 10556, Streptococcus gordonii ATCC 10558, Porphyromonas gingivalis W83 and Prevotella intermedia ATCC 49046 were cultivated in TYGVS medium [22], while T. forsythia ATCC 43037 was grown in new oral spirochete (NOS) medium supplemented with vitamin K (0.2 mg/ml) and N-acetylmuramic acid (0.01 mg/ml) [23]

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Summary

Introduction

T. denticola is considered to be a significant contributor to periodontal disease and its abundance is highly correlated with periodontal pocket depth, an important indicator of disease severity [1,2,3]. Advances have been made in understanding signaling events in T. denticola triggered by environmental conditions associated with periodontal disease [5,6,7], the molecular mechanisms associated with its response to other oral bacterial species are largely unknown. This anaerobic spirochete is a member of the ‘‘red complex’’, which is comprised of T. denticola, T. forsythia, as well as P. gingivalis [8,9,10]. Red complex organisms were found to be highly correlated with periodontal lesions [10], thrive in close contact with each other and exhibit synergistic relationships [11,12]. T. denticola does not attach to early colonizing Streptococci (yellow complex) and requires interaction with bridging organisms such as F. nucleatum and P

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