Relationship between expression of the family of M proteins and lipoteichoic acid to hydrophobicity and biofilm formation in Streptococcus pyogenes.

<h4>Background</h4>Hydrophobicity is an important attribute of bacteria that contributes to adhesion and biofilm formation. Hydrophobicity of Streptococcus pyogenes is primarily due to lipoteichoic acid (LTA) on the streptococcal surface but the mechanism(s) whereby LTA is retained on th...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Harry S Courtney, Itzhak Ofek, Thomas Penfound, Victor Nizet, Morgan A Pence, Bernd Kreikemeyer, Andreas Podbielski, David L Hasty, James B Dale
Formato: article
Lenguaje:EN
Publicado: Public Library of Science (PLoS) 2009
Materias:
R
Q
Acceso en línea:https://doaj.org/article/c25d60e84c374d7ea659406e8a7a68d0
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:c25d60e84c374d7ea659406e8a7a68d0
record_format dspace
spelling oai:doaj.org-article:c25d60e84c374d7ea659406e8a7a68d02021-11-25T06:17:49ZRelationship between expression of the family of M proteins and lipoteichoic acid to hydrophobicity and biofilm formation in Streptococcus pyogenes.1932-620310.1371/journal.pone.0004166https://doaj.org/article/c25d60e84c374d7ea659406e8a7a68d02009-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/19132104/pdf/?tool=EBIhttps://doaj.org/toc/1932-6203<h4>Background</h4>Hydrophobicity is an important attribute of bacteria that contributes to adhesion and biofilm formation. Hydrophobicity of Streptococcus pyogenes is primarily due to lipoteichoic acid (LTA) on the streptococcal surface but the mechanism(s) whereby LTA is retained on the surface is poorly understood. In this study, we sought to determine whether members of the M protein family consisting of Emm (M protein), Mrp (M-related protein), Enn (an M-like protein), and the streptococcal protective antigen (Spa) are involved in anchoring LTA in a manner that contributes to hydrophobicity of the streptococci and its ability to form biofilms.<h4>Methodology/principal findings</h4>Isogenic mutants defective in expression of emm, mrp, enn, and/or spa genes of eight different serotypes and their parental strains were tested for differences in LTA bound to surface proteins, LTA released into the culture media, and membrane-bound LTA. The effect of these mutations on the ability of streptococci to form a hydrophobic surface and to generate biofilms was also investigated. A recombinant strain overexpressing Emm1 was also engineered and similarly tested. The serotypes tested ranged from those that express only a single M protein gene to those that express two or three members of the M protein family. Overexpression of Emm1 led to enhanced hydrophobicity and biofilm formation. Inactivation of emm in those serotypes expressing only a single emm gene reduced biofilm formation, and protein-bound LTA on the surface, but did not alter the levels of membrane-bound LTA. The results were more varied in those serotypes that express two to three members of the M protein family.<h4>Conclusions/significance</h4>Our findings suggest that the formation of complexes with members of the M protein family is a common mechanism for anchoring LTA on the surface in a manner that contributes to hydrophobicity and to biofilm formation in S. pyogenes, but these activities in some serotypes are dependent on a trypsin-sensitive protein(s) that remains to be identified. The need for interactions between LTA and M proteins may impose functional constraints that limit variations in the sequence of the M proteins, major virulence factors of S. pyogenes.Harry S CourtneyItzhak OfekThomas PenfoundVictor NizetMorgan A PenceBernd KreikemeyerAndreas PodbielskiDavid L HastyJames B DalePublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 4, Iss 1, p e4166 (2009)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Harry S Courtney
Itzhak Ofek
Thomas Penfound
Victor Nizet
Morgan A Pence
Bernd Kreikemeyer
Andreas Podbielski
David L Hasty
James B Dale
Relationship between expression of the family of M proteins and lipoteichoic acid to hydrophobicity and biofilm formation in Streptococcus pyogenes.
description <h4>Background</h4>Hydrophobicity is an important attribute of bacteria that contributes to adhesion and biofilm formation. Hydrophobicity of Streptococcus pyogenes is primarily due to lipoteichoic acid (LTA) on the streptococcal surface but the mechanism(s) whereby LTA is retained on the surface is poorly understood. In this study, we sought to determine whether members of the M protein family consisting of Emm (M protein), Mrp (M-related protein), Enn (an M-like protein), and the streptococcal protective antigen (Spa) are involved in anchoring LTA in a manner that contributes to hydrophobicity of the streptococci and its ability to form biofilms.<h4>Methodology/principal findings</h4>Isogenic mutants defective in expression of emm, mrp, enn, and/or spa genes of eight different serotypes and their parental strains were tested for differences in LTA bound to surface proteins, LTA released into the culture media, and membrane-bound LTA. The effect of these mutations on the ability of streptococci to form a hydrophobic surface and to generate biofilms was also investigated. A recombinant strain overexpressing Emm1 was also engineered and similarly tested. The serotypes tested ranged from those that express only a single M protein gene to those that express two or three members of the M protein family. Overexpression of Emm1 led to enhanced hydrophobicity and biofilm formation. Inactivation of emm in those serotypes expressing only a single emm gene reduced biofilm formation, and protein-bound LTA on the surface, but did not alter the levels of membrane-bound LTA. The results were more varied in those serotypes that express two to three members of the M protein family.<h4>Conclusions/significance</h4>Our findings suggest that the formation of complexes with members of the M protein family is a common mechanism for anchoring LTA on the surface in a manner that contributes to hydrophobicity and to biofilm formation in S. pyogenes, but these activities in some serotypes are dependent on a trypsin-sensitive protein(s) that remains to be identified. The need for interactions between LTA and M proteins may impose functional constraints that limit variations in the sequence of the M proteins, major virulence factors of S. pyogenes.
format article
author Harry S Courtney
Itzhak Ofek
Thomas Penfound
Victor Nizet
Morgan A Pence
Bernd Kreikemeyer
Andreas Podbielski
David L Hasty
James B Dale
author_facet Harry S Courtney
Itzhak Ofek
Thomas Penfound
Victor Nizet
Morgan A Pence
Bernd Kreikemeyer
Andreas Podbielski
David L Hasty
James B Dale
author_sort Harry S Courtney
title Relationship between expression of the family of M proteins and lipoteichoic acid to hydrophobicity and biofilm formation in Streptococcus pyogenes.
title_short Relationship between expression of the family of M proteins and lipoteichoic acid to hydrophobicity and biofilm formation in Streptococcus pyogenes.
title_full Relationship between expression of the family of M proteins and lipoteichoic acid to hydrophobicity and biofilm formation in Streptococcus pyogenes.
title_fullStr Relationship between expression of the family of M proteins and lipoteichoic acid to hydrophobicity and biofilm formation in Streptococcus pyogenes.
title_full_unstemmed Relationship between expression of the family of M proteins and lipoteichoic acid to hydrophobicity and biofilm formation in Streptococcus pyogenes.
title_sort relationship between expression of the family of m proteins and lipoteichoic acid to hydrophobicity and biofilm formation in streptococcus pyogenes.
publisher Public Library of Science (PLoS)
publishDate 2009
url https://doaj.org/article/c25d60e84c374d7ea659406e8a7a68d0
work_keys_str_mv AT harryscourtney relationshipbetweenexpressionofthefamilyofmproteinsandlipoteichoicacidtohydrophobicityandbiofilmformationinstreptococcuspyogenes
AT itzhakofek relationshipbetweenexpressionofthefamilyofmproteinsandlipoteichoicacidtohydrophobicityandbiofilmformationinstreptococcuspyogenes
AT thomaspenfound relationshipbetweenexpressionofthefamilyofmproteinsandlipoteichoicacidtohydrophobicityandbiofilmformationinstreptococcuspyogenes
AT victornizet relationshipbetweenexpressionofthefamilyofmproteinsandlipoteichoicacidtohydrophobicityandbiofilmformationinstreptococcuspyogenes
AT morganapence relationshipbetweenexpressionofthefamilyofmproteinsandlipoteichoicacidtohydrophobicityandbiofilmformationinstreptococcuspyogenes
AT berndkreikemeyer relationshipbetweenexpressionofthefamilyofmproteinsandlipoteichoicacidtohydrophobicityandbiofilmformationinstreptococcuspyogenes
AT andreaspodbielski relationshipbetweenexpressionofthefamilyofmproteinsandlipoteichoicacidtohydrophobicityandbiofilmformationinstreptococcuspyogenes
AT davidlhasty relationshipbetweenexpressionofthefamilyofmproteinsandlipoteichoicacidtohydrophobicityandbiofilmformationinstreptococcuspyogenes
AT jamesbdale relationshipbetweenexpressionofthefamilyofmproteinsandlipoteichoicacidtohydrophobicityandbiofilmformationinstreptococcuspyogenes
_version_ 1718413951004311552