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Front. Microbiol. | doi: 10.3389/fmicb.2018.00273

Identification of new factors modulating adhesion abilities of the pioneer commensal bacterium Streptococcus salivarius

  • 1Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, France
  • 2Metagenopolis, INRA, Université Paris-Saclay, France
  • 3MaIAGE, INRA, Université Paris-Saclay, France
  • 4Microscopie et Imagerie des Micro-organismes, Animaux et Aliments (MIMA2), France
  • 5INRA UMR1253 Science & technologie du lait & de l'œuf, France

Biofilm formation is crucial for bacterial community development and host colonization by Streptococcus salivarius, a pioneer colonizer and commensal bacterium of the human gastrointestinal tract. This ability to form biofilms depends on bacterial adhesion to host surfaces, and on the intercellular aggregation contributing to biofilm cohesiveness. Many S. salivarius isolates auto-aggregate, an adhesion process mediated by cell surface proteins. To gain an insight into the genetic factors of S. salivarius that dictate host adhesion and biofilm formation, we developed a screening method, based on the differential sedimentation of bacteria in semi-liquid conditions according to their auto-aggregation capacity, which allowed us to identify twelve mutations affecting this auto-aggregation phenotype. Mutations targeted genes encoding (i) extracellular components, including the CshA surface-exposed protein, the extracellular BglB glucan-binding protein, the GtfE, GtfG and GtfH glycosyltransferases and enzymes responsible for synthesis of cell wall polysaccharides (CwpB, CwpK), (ii) proteins responsible for the extracellular localization of proteins, such as structural components of the accessory SecA2Y2 system (Asp1, Asp2, SecA2) and the SrtA sortase, and (iii) the LiaR transcriptional response regulator. These mutations also influenced biofilm architecture, revealing that similar cell-to-cell interactions govern assembly of auto-aggregates and biofilm formation. We found that BglB, CshA, GtfH and LiaR were specifically associated with bacterial auto-aggregation, whereas Asp1, Asp2, CwpB, CwpK, GtfE, GtfG, SecA2 and SrtA also contributed to adhesion to host cells and host-derived components, or to interactions with the human pathogen Fusobacterium nucleatum. Our study demonstrates that our screening method could also be used to identify genes implicated in the bacterial interactions of pathogens or probiotics, for which aggregation is either a virulence trait or an advantageous feature, respectively.

Keywords: Adhesion gene, Biofilm formation, Aggregation, host interactions, Sedimentation, commensal bacteria, Streptococcus salivarius

Received: 22 Nov 2017; Accepted: 06 Feb 2018.

Edited by:

Baolei Jia, Chung-Ang University, South Korea

Reviewed by:

Tom Reese, National Institutes of Health (NIH), United States
Sarah Maddocks, Cardiff Metropolitan University, United Kingdom
Cheorl-Ho Kim, Sungkyunkwan University, South Korea  

Copyright: © 2018 Couvigny, Kulakauskas, Pons, Quinquis, Abraham, Meylheuc, Delorme, Renault, Briandet, Lapaque and Guédon. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: PhD. Eric Guédon, INRA UMR1253 Science & technologie du lait & de l'œuf, Rennes, France, eric.guedon@inra.fr