A Low-Abundance Biofilm Species Orchestrates Inflammatory Periodontal Disease through the Commensal Microbiota and the Complement Pathway

By G. Hajishengallis, S. Liang, M. Payne, A. Hashim, R. Jotwani, M. Eskan, Megan L. McIntosh, A. Alsam, K. Kirkwood, John D Lambris and 2 more. Cell Host and Microbe, 2011

1,111 citations recorded by the source corpus.

SUMMARY Porphyromonas gingivalis is a low-abundance oral anaerobic bacterium implicated in periodontitis, a polymicrobial inflammatory disease, and the associated systemic conditions. However, the mechanism by which P. gingivalis contributes to inflammation and disease has remained elusive. Here we show that P. gingivalis, at very low colonization levels, triggers changes to the amount and composition of the oral commensal microbiota leading to inflammatory periodontal bone loss. The commensal microbiota and the complement pathway were both required for P. gingivalis-induced bone loss as germ-free mice or conventionally raised C3a and C5a receptor deficient mice did not develop bone loss after inoculation with P. gingivalis. These findings demonstrate that a single, low-abundance species can disrupt host-microbial homeostasis to cause inflammatory disease. The identification and targeting of similar low-abundance pathogens with community-wide impact may be important for treating inflammatory diseases of polymicrobial etiology.

Subfields: Periodontics, Physiology, Public Health, Environmental and Occupational Health

View Paper: https://www.semanticscholar.org/paper/2d01ab1f9c6c0cd419979a481b087e27d7b99c67

How researchers see this paper

The researchers whose trusted networks rank it highest, strongest advocate first. Every researcher gets a different order.

In Periodontics

1. G. Hajishengallis
2. R. J. Lamont
3. Patricia I. Diaz

In Physiology

1. G. Hajishengallis
2. R. J. Lamont
3. Steven G. Deeks
4. W. Garrett

In Public Health, Environmental and Occupational Health

1. R. J. Lamont
2. Patricia I. Diaz

Citations in the corpus

• Where less may be more: how the rare biosphere pulls ecosystems strings (2017, background): “Conversely, rare species may contribute to pathogenesis, as shown by the initiation of periodontal disease by low-abundance species that trigger changes in the oral microflora (Hajishengallis et al., 2011).”
• Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology (2012, positive): “N IH -PA Author M anuscript N IH -PA Author M anuscript N IH -PA Author M anuscript pathogenic influence on the microbiota in animals, at least in part via host modulation (Hajishengallis et al., 2011).”
• Human Intestinal Lumen and Mucosa-Associated Microbiota in Patients with Colorectal Cancer (2012, background): “gingivalis, a main species of Porphyromonas, penetrates periodontal tissue, disrupt the host cell activity, and alters the microbiota composition to induce periodontitis [48,49,50].”
• The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation (2013, background): “Recent studies in mice demonstrated that, low-levels of colonization by periodontitis-associated microorganisms such as Porphyromonas gingivalis are sufficient to dysregulate innate immunity pathways, facilitate an increase in overall community biomass and trigger periodontal destruction (Hajishenga”
• Fap2 Mediates Fusobacterium nucleatum Colorectal Adenocarcinoma Enrichment by Binding to Tumor-Expressed Gal-GalNAc (2016, background): “Porphyromonas gingivalis, is an oral Gram-negative, anaerobic periodontal bacterium (Hajishengallis et al., 2011) that was previously found to be overabundant in gingival squamous cell carcinoma (Gao et al., 2016; Katz et al., 2011; Whitmore and Lamont, 2014).”
• Dysbiosis of the Gut Microbiota Is Associated with HIV Disease Progression and Tryptophan Catabolism (2013, background): “This is particularly relevant given recent evidencedemonstrating thepresenceof low-abundance “keystone” species that, despite their low numbers, are pivotal in modulating commensal community composition and host-microbe interactions in the oral cavity (31).”
• The human microbiome (2017, background): “Small quantities of this bacterium were shown to induce changes in the oral microbiota by exploiting the complement cascade to cause periodontal bone loss [37].”