Dual role for pilus in adherence to epithelial cells and biofilm formation in Streptococcus agalactiae.

Streptococcus agalactiae is a common human commensal and a major life-threatening pathogen in neonates. Adherence to host epithelial cells is the first critical step of the infectious process. Pili have been observed on the surface of several gram-positive bacteria including S. agalactiae. We previo...

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Autores principales:	Yoan Konto-Ghiorghi, Emilie Mairey, Adeline Mallet, Guillaume Duménil, Elise Caliot, Patrick Trieu-Cuot, Shaynoor Dramsi
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2009
Materias:	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/b60477d291964540857050f0d20ff622
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spelling	oai:doaj.org-article:b60477d291964540857050f0d20ff6222021-11-25T05:47:56ZDual role for pilus in adherence to epithelial cells and biofilm formation in Streptococcus agalactiae.1553-73661553-737410.1371/journal.ppat.1000422https://doaj.org/article/b60477d291964540857050f0d20ff6222009-05-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/19424490/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Streptococcus agalactiae is a common human commensal and a major life-threatening pathogen in neonates. Adherence to host epithelial cells is the first critical step of the infectious process. Pili have been observed on the surface of several gram-positive bacteria including S. agalactiae. We previously characterized the pilus-encoding operon gbs1479-1474 in strain NEM316. This pilus is composed of three structural subunit proteins: Gbs1478 (PilA), Gbs1477 (PilB), and Gbs1474 (PilC), and its assembly involves two class C sortases (SrtC3 and SrtC4). PilB, the bona fide pilin, is the major component; PilA, the pilus associated adhesin, and PilC, are both accessory proteins incorporated into the pilus backbone. We first addressed the role of the housekeeping sortase A in pilus biogenesis and showed that it is essential for the covalent anchoring of the pilus fiber to the peptidoglycan. We next aimed at understanding the role of the pilus fiber in bacterial adherence and at resolving the paradox of an adhesive but dispensable pilus. Combining immunoblotting and electron microscopy analyses, we showed that the PilB fiber is essential for efficient PilA display on the surface of the capsulated strain NEM316. We then demonstrated that pilus integrity becomes critical for adherence to respiratory epithelial cells under flow-conditions mimicking an in vivo situation and revealing the limitations of the commonly used static adherence model. Interestingly, PilA exhibits a von Willebrand adhesion domain (VWA) found in many extracellular eucaryotic proteins. We show here that the VWA domain of PilA is essential for its adhesive function, demonstrating for the first time the functionality of a prokaryotic VWA homolog. Furthermore, the auto aggregative phenotype of NEM316 observed in standing liquid culture was strongly reduced in all three individual pilus mutants. S. agalactiae strain NEM316 was able to form biofilm in microtiter plate and, strikingly, the PilA and PilB mutants were strongly impaired in biofilm formation. Surprisingly, the VWA domain involved in adherence to epithelial cells was not required for biofilm formation.Yoan Konto-GhiorghiEmilie MaireyAdeline MalletGuillaume DuménilElise CaliotPatrick Trieu-CuotShaynoor DramsiPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 5, Iss 5, p e1000422 (2009)
institution	DOAJ
collection	DOAJ
language	EN
topic	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
spellingShingle	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Yoan Konto-Ghiorghi Emilie Mairey Adeline Mallet Guillaume Duménil Elise Caliot Patrick Trieu-Cuot Shaynoor Dramsi Dual role for pilus in adherence to epithelial cells and biofilm formation in Streptococcus agalactiae.
description	Streptococcus agalactiae is a common human commensal and a major life-threatening pathogen in neonates. Adherence to host epithelial cells is the first critical step of the infectious process. Pili have been observed on the surface of several gram-positive bacteria including S. agalactiae. We previously characterized the pilus-encoding operon gbs1479-1474 in strain NEM316. This pilus is composed of three structural subunit proteins: Gbs1478 (PilA), Gbs1477 (PilB), and Gbs1474 (PilC), and its assembly involves two class C sortases (SrtC3 and SrtC4). PilB, the bona fide pilin, is the major component; PilA, the pilus associated adhesin, and PilC, are both accessory proteins incorporated into the pilus backbone. We first addressed the role of the housekeeping sortase A in pilus biogenesis and showed that it is essential for the covalent anchoring of the pilus fiber to the peptidoglycan. We next aimed at understanding the role of the pilus fiber in bacterial adherence and at resolving the paradox of an adhesive but dispensable pilus. Combining immunoblotting and electron microscopy analyses, we showed that the PilB fiber is essential for efficient PilA display on the surface of the capsulated strain NEM316. We then demonstrated that pilus integrity becomes critical for adherence to respiratory epithelial cells under flow-conditions mimicking an in vivo situation and revealing the limitations of the commonly used static adherence model. Interestingly, PilA exhibits a von Willebrand adhesion domain (VWA) found in many extracellular eucaryotic proteins. We show here that the VWA domain of PilA is essential for its adhesive function, demonstrating for the first time the functionality of a prokaryotic VWA homolog. Furthermore, the auto aggregative phenotype of NEM316 observed in standing liquid culture was strongly reduced in all three individual pilus mutants. S. agalactiae strain NEM316 was able to form biofilm in microtiter plate and, strikingly, the PilA and PilB mutants were strongly impaired in biofilm formation. Surprisingly, the VWA domain involved in adherence to epithelial cells was not required for biofilm formation.
format	article
author	Yoan Konto-Ghiorghi Emilie Mairey Adeline Mallet Guillaume Duménil Elise Caliot Patrick Trieu-Cuot Shaynoor Dramsi
author_facet	Yoan Konto-Ghiorghi Emilie Mairey Adeline Mallet Guillaume Duménil Elise Caliot Patrick Trieu-Cuot Shaynoor Dramsi
author_sort	Yoan Konto-Ghiorghi
title	Dual role for pilus in adherence to epithelial cells and biofilm formation in Streptococcus agalactiae.
title_short	Dual role for pilus in adherence to epithelial cells and biofilm formation in Streptococcus agalactiae.
title_full	Dual role for pilus in adherence to epithelial cells and biofilm formation in Streptococcus agalactiae.
title_fullStr	Dual role for pilus in adherence to epithelial cells and biofilm formation in Streptococcus agalactiae.
title_full_unstemmed	Dual role for pilus in adherence to epithelial cells and biofilm formation in Streptococcus agalactiae.
title_sort	dual role for pilus in adherence to epithelial cells and biofilm formation in streptococcus agalactiae.
publisher	Public Library of Science (PLoS)
publishDate	2009
url	https://doaj.org/article/b60477d291964540857050f0d20ff622
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Dual role for pilus in adherence to epithelial cells and biofilm formation in Streptococcus agalactiae.

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