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Uncovering the link between the SpnIII restriction modification system and LuxS in Streptococcus pneumoniae meningitis isolates

Streptococcus pneumoniae is capable of randomly switching their genomic DNA methylation pattern between six distinct bacterial subpopulations (A-F) via recombination of a type 1 restriction-modification locus, spnIII. These pneumococcal subpopulations exhibit phenotypic changes which favor carriage...

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Autores principales: Agnew, Hannah N., Atack, John M., Fernando, Ann R.D., Waters, Sophie N., van der Linden, Mark, Smith, Erin, Abell, Andrew D., Brazel, Erin B., Paton, James C., Trappetti, Claudia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10184825/
https://www.ncbi.nlm.nih.gov/pubmed/37197203
http://dx.doi.org/10.3389/fcimb.2023.1177857
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author Agnew, Hannah N.
Atack, John M.
Fernando, Ann R.D.
Waters, Sophie N.
van der Linden, Mark
Smith, Erin
Abell, Andrew D.
Brazel, Erin B.
Paton, James C.
Trappetti, Claudia
author_facet Agnew, Hannah N.
Atack, John M.
Fernando, Ann R.D.
Waters, Sophie N.
van der Linden, Mark
Smith, Erin
Abell, Andrew D.
Brazel, Erin B.
Paton, James C.
Trappetti, Claudia
author_sort Agnew, Hannah N.
collection PubMed
description Streptococcus pneumoniae is capable of randomly switching their genomic DNA methylation pattern between six distinct bacterial subpopulations (A-F) via recombination of a type 1 restriction-modification locus, spnIII. These pneumococcal subpopulations exhibit phenotypic changes which favor carriage or invasive disease. In particular, the spnIIIB allele has been associated with increased nasopharyngeal carriage and the downregulation of the luxS gene. The LuxS/AI-2 QS system represent a universal language for bacteria and has been linked to virulence and biofilm formation in S. pneumoniae. In this work, we have explored the link between spnIII alleles, the luxS gene and virulence in two clinical pneumococcal isolates from the blood and cerebrospinal fluid (CSF) of one pediatric meningitis patient. The blood and CSF strains showed different virulence profiles in mice. Analysis of the spnIII system of these strains recovered from the murine nasopharynx showed that the system switched to different alleles commensurate with the initial source of the isolate. Of note, the blood strain showed high expression of spnIIIB allele, previously linked with less LuxS protein production. Importantly, strains with deleted luxS displayed different phenotypic profiles compared to the wildtype, but similar to the strains recovered from the nasopharynx of infected mice. This study used clinically relevant S. pneumoniae strains to demonstrate that the regulatory network between luxS and the type 1 restriction-modification system play a key role in infections and may support different adaptation to specific host niches.
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spelling pubmed-101848252023-05-16 Uncovering the link between the SpnIII restriction modification system and LuxS in Streptococcus pneumoniae meningitis isolates Agnew, Hannah N. Atack, John M. Fernando, Ann R.D. Waters, Sophie N. van der Linden, Mark Smith, Erin Abell, Andrew D. Brazel, Erin B. Paton, James C. Trappetti, Claudia Front Cell Infect Microbiol Cellular and Infection Microbiology Streptococcus pneumoniae is capable of randomly switching their genomic DNA methylation pattern between six distinct bacterial subpopulations (A-F) via recombination of a type 1 restriction-modification locus, spnIII. These pneumococcal subpopulations exhibit phenotypic changes which favor carriage or invasive disease. In particular, the spnIIIB allele has been associated with increased nasopharyngeal carriage and the downregulation of the luxS gene. The LuxS/AI-2 QS system represent a universal language for bacteria and has been linked to virulence and biofilm formation in S. pneumoniae. In this work, we have explored the link between spnIII alleles, the luxS gene and virulence in two clinical pneumococcal isolates from the blood and cerebrospinal fluid (CSF) of one pediatric meningitis patient. The blood and CSF strains showed different virulence profiles in mice. Analysis of the spnIII system of these strains recovered from the murine nasopharynx showed that the system switched to different alleles commensurate with the initial source of the isolate. Of note, the blood strain showed high expression of spnIIIB allele, previously linked with less LuxS protein production. Importantly, strains with deleted luxS displayed different phenotypic profiles compared to the wildtype, but similar to the strains recovered from the nasopharynx of infected mice. This study used clinically relevant S. pneumoniae strains to demonstrate that the regulatory network between luxS and the type 1 restriction-modification system play a key role in infections and may support different adaptation to specific host niches. Frontiers Media S.A. 2023-05-01 /pmc/articles/PMC10184825/ /pubmed/37197203 http://dx.doi.org/10.3389/fcimb.2023.1177857 Text en Copyright © 2023 Agnew, Atack, Fernando, Waters, van der Linden, Smith, Abell, Brazel, Paton and Trappetti https://creativecommons.org/licenses/by/4.0/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(s) 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.
spellingShingle Cellular and Infection Microbiology
Agnew, Hannah N.
Atack, John M.
Fernando, Ann R.D.
Waters, Sophie N.
van der Linden, Mark
Smith, Erin
Abell, Andrew D.
Brazel, Erin B.
Paton, James C.
Trappetti, Claudia
Uncovering the link between the SpnIII restriction modification system and LuxS in Streptococcus pneumoniae meningitis isolates
title Uncovering the link between the SpnIII restriction modification system and LuxS in Streptococcus pneumoniae meningitis isolates
title_full Uncovering the link between the SpnIII restriction modification system and LuxS in Streptococcus pneumoniae meningitis isolates
title_fullStr Uncovering the link between the SpnIII restriction modification system and LuxS in Streptococcus pneumoniae meningitis isolates
title_full_unstemmed Uncovering the link between the SpnIII restriction modification system and LuxS in Streptococcus pneumoniae meningitis isolates
title_short Uncovering the link between the SpnIII restriction modification system and LuxS in Streptococcus pneumoniae meningitis isolates
title_sort uncovering the link between the spniii restriction modification system and luxs in streptococcus pneumoniae meningitis isolates
topic Cellular and Infection Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10184825/
https://www.ncbi.nlm.nih.gov/pubmed/37197203
http://dx.doi.org/10.3389/fcimb.2023.1177857
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