Polymicrobial synergy within oral biofilm promotes invasion of dendritic cells and survival of consortia members

Ahmed El-Awady, Mariana de Sousa Rabelo, Mohamed M. Meghil, Mythilypriya Rajendran, Mahmoud Elashiry, Amanda Finger Stadler, Adriana Moura Foz, Cristiano Susin, Giuseppe Alexandre Romito, Roger Mauricio Arce Munoz, Christopher W Cutler

Research output: Contribution to journalArticle

Abstract

Years of human microbiome research have confirmed that microbes rarely live or function alone, favoring diverse communities. Yet most experimental host-pathogen studies employ single species models of infection. Here, the influence of three-species oral microbial consortium on growth, virulence, invasion and persistence in dendritic cells (DCs) was examined experimentally in human monocyte-derived dendritic cells (DCs) and in patients with periodontitis (PD). Cooperative biofilm formation by Streptococcus gordonii, Fusobacterium nucleatum and Porphyromonas gingivalis was documented in vitro using growth models and scanning electron microscopy. Analysis of growth rates by species-specific 16s rRNA probes revealed distinct, early advantages to consortium growth for S. gordonii and F. nucleatum with P. gingivalis, while P. gingivalis upregulated its short mfa1 fimbriae, leading to increased invasion of DCs. F. nucleatum was only taken up by DCs when in consortium with P. gingivalis. Mature consortium regressed DC maturation upon uptake, as determined by flow cytometry. Analysis of dental plaques of PD and healthy subjects by 16s rRNA confirmed oral colonization with consortium members, but DC hematogenous spread was limited to P. gingivalis and F. nucleatum. Expression of P. gingivalis mfa1 fimbriae was increased in dental plaques and hematogenous DCs of PD patients. P. gingivalis in the consortium correlated with an adverse clinical response in the gingiva of PD subjects. In conclusion, we have identified polymicrobial synergy in a three-species oral consortium that may have negative consequences for the host, including microbial dissemination and adverse peripheral inflammatory responses.

Original languageEnglish (US)
Article number11
Journalnpj Biofilms and Microbiomes
Volume5
Issue number1
DOIs
StatePublished - Dec 1 2019

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Porphyromonas gingivalis
Biofilms
Dendritic Cells
Cell Survival
Fusobacterium nucleatum
Periodontitis
Streptococcus gordonii
Dental Plaque
Growth
Microbial Consortia
Microbiota
Gingiva
Electron Scanning Microscopy
Virulence
Monocytes
Healthy Volunteers
Flow Cytometry
Infection
Research

ASJC Scopus subject areas

  • Biotechnology
  • Microbiology
  • Applied Microbiology and Biotechnology

Cite this

Polymicrobial synergy within oral biofilm promotes invasion of dendritic cells and survival of consortia members. / El-Awady, Ahmed; de Sousa Rabelo, Mariana; Meghil, Mohamed M.; Rajendran, Mythilypriya; Elashiry, Mahmoud; Stadler, Amanda Finger; Foz, Adriana Moura; Susin, Cristiano; Romito, Giuseppe Alexandre; Arce Munoz, Roger Mauricio; Cutler, Christopher W.

In: npj Biofilms and Microbiomes, Vol. 5, No. 1, 11, 01.12.2019.

Research output: Contribution to journalArticle

El-Awady, A, de Sousa Rabelo, M, Meghil, MM, Rajendran, M, Elashiry, M, Stadler, AF, Foz, AM, Susin, C, Romito, GA, Arce Munoz, RM & Cutler, CW 2019, 'Polymicrobial synergy within oral biofilm promotes invasion of dendritic cells and survival of consortia members', npj Biofilms and Microbiomes, vol. 5, no. 1, 11. https://doi.org/10.1038/s41522-019-0084-7
El-Awady, Ahmed ; de Sousa Rabelo, Mariana ; Meghil, Mohamed M. ; Rajendran, Mythilypriya ; Elashiry, Mahmoud ; Stadler, Amanda Finger ; Foz, Adriana Moura ; Susin, Cristiano ; Romito, Giuseppe Alexandre ; Arce Munoz, Roger Mauricio ; Cutler, Christopher W. / Polymicrobial synergy within oral biofilm promotes invasion of dendritic cells and survival of consortia members. In: npj Biofilms and Microbiomes. 2019 ; Vol. 5, No. 1.
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