Remodeling of the Z-Ring Nanostructure during the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Cell Cycle Revealed by Photoactivated Localization Microscopy

ABSTRACT Ovococci form a morphological group that includes several human pathogens (enterococci and streptococci). Their shape results from two modes of cell wall insertion, one allowing division and one allowing elongation. Both cell wall synthesis modes rely on a single cytoskeletal protein, FtsZ....

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Autores principales:	Maxime Jacq, Virgile Adam, Dominique Bourgeois, Christine Moriscot, Anne-Marie Di Guilmi, Thierry Vernet, Cécile Morlot
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/853c889d41384c5d90b7073ad431744e
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spelling	oai:doaj.org-article:853c889d41384c5d90b7073ad431744e2021-11-15T15:41:26ZRemodeling of the Z-Ring Nanostructure during the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Cell Cycle Revealed by Photoactivated Localization Microscopy10.1128/mBio.01108-152150-7511https://doaj.org/article/853c889d41384c5d90b7073ad431744e2015-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01108-15https://doaj.org/toc/2150-7511ABSTRACT Ovococci form a morphological group that includes several human pathogens (enterococci and streptococci). Their shape results from two modes of cell wall insertion, one allowing division and one allowing elongation. Both cell wall synthesis modes rely on a single cytoskeletal protein, FtsZ. Despite the central role of FtsZ in ovococci, a detailed view of the in vivo nanostructure of ovococcal Z-rings has been lacking thus far, limiting our understanding of their assembly and architecture. We have developed the use of photoactivated localization microscopy (PALM) in the ovococcus human pathogen Streptococcus pneumoniae by engineering spDendra2, a photoconvertible fluorescent protein optimized for this bacterium. Labeling of endogenously expressed FtsZ with spDendra2 revealed the remodeling of the Z-ring's morphology during the division cycle at the nanoscale level. We show that changes in the ring's axial thickness and in the clustering propensity of FtsZ correlate with the advancement of the cell cycle. In addition, we observe double-ring substructures suggestive of short-lived intermediates that may form upon initiation of septal cell wall synthesis. These data are integrated into a model describing the architecture and the remodeling of the Z-ring during the cell cycle of ovococci. IMPORTANCE The Gram-positive human pathogen S. pneumoniae is responsible for 1.6 million deaths per year worldwide and is increasingly resistant to various antibiotics. FtsZ is a cytoskeletal protein polymerizing at midcell into a ring-like structure called the Z-ring. FtsZ is a promising new antimicrobial target, as its inhibition leads to cell death. A precise view of the Z-ring architecture in vivo is essential to understand the mode of action of inhibitory drugs (see T. den Blaauwen, J. M. Andreu, and O. Monasterio, Bioorg Chem 55:27–38, 2014, doi:10.1016/j.bioorg.2014.03.007, for a review on FtsZ inhibitors). This is notably true in ovococcoid bacteria like S. pneumoniae, in which FtsZ is the only known cytoskeletal protein. We have used superresolution microscopy to obtain molecular details of the pneumococcus Z-ring that have so far been inaccessible with conventional microscopy. This study provides a nanoscale description of the Z-ring architecture and remodeling during the division of ovococci.Maxime JacqVirgile AdamDominique BourgeoisChristine MoriscotAnne-Marie Di GuilmiThierry VernetCécile MorlotAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 4 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Maxime Jacq Virgile Adam Dominique Bourgeois Christine Moriscot Anne-Marie Di Guilmi Thierry Vernet Cécile Morlot Remodeling of the Z-Ring Nanostructure during the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Cell Cycle Revealed by Photoactivated Localization Microscopy
description	ABSTRACT Ovococci form a morphological group that includes several human pathogens (enterococci and streptococci). Their shape results from two modes of cell wall insertion, one allowing division and one allowing elongation. Both cell wall synthesis modes rely on a single cytoskeletal protein, FtsZ. Despite the central role of FtsZ in ovococci, a detailed view of the in vivo nanostructure of ovococcal Z-rings has been lacking thus far, limiting our understanding of their assembly and architecture. We have developed the use of photoactivated localization microscopy (PALM) in the ovococcus human pathogen Streptococcus pneumoniae by engineering spDendra2, a photoconvertible fluorescent protein optimized for this bacterium. Labeling of endogenously expressed FtsZ with spDendra2 revealed the remodeling of the Z-ring's morphology during the division cycle at the nanoscale level. We show that changes in the ring's axial thickness and in the clustering propensity of FtsZ correlate with the advancement of the cell cycle. In addition, we observe double-ring substructures suggestive of short-lived intermediates that may form upon initiation of septal cell wall synthesis. These data are integrated into a model describing the architecture and the remodeling of the Z-ring during the cell cycle of ovococci. IMPORTANCE The Gram-positive human pathogen S. pneumoniae is responsible for 1.6 million deaths per year worldwide and is increasingly resistant to various antibiotics. FtsZ is a cytoskeletal protein polymerizing at midcell into a ring-like structure called the Z-ring. FtsZ is a promising new antimicrobial target, as its inhibition leads to cell death. A precise view of the Z-ring architecture in vivo is essential to understand the mode of action of inhibitory drugs (see T. den Blaauwen, J. M. Andreu, and O. Monasterio, Bioorg Chem 55:27–38, 2014, doi:10.1016/j.bioorg.2014.03.007, for a review on FtsZ inhibitors). This is notably true in ovococcoid bacteria like S. pneumoniae, in which FtsZ is the only known cytoskeletal protein. We have used superresolution microscopy to obtain molecular details of the pneumococcus Z-ring that have so far been inaccessible with conventional microscopy. This study provides a nanoscale description of the Z-ring architecture and remodeling during the division of ovococci.
format	article
author	Maxime Jacq Virgile Adam Dominique Bourgeois Christine Moriscot Anne-Marie Di Guilmi Thierry Vernet Cécile Morlot
author_facet	Maxime Jacq Virgile Adam Dominique Bourgeois Christine Moriscot Anne-Marie Di Guilmi Thierry Vernet Cécile Morlot
author_sort	Maxime Jacq
title	Remodeling of the Z-Ring Nanostructure during the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Cell Cycle Revealed by Photoactivated Localization Microscopy
title_short	Remodeling of the Z-Ring Nanostructure during the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Cell Cycle Revealed by Photoactivated Localization Microscopy
title_full	Remodeling of the Z-Ring Nanostructure during the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Cell Cycle Revealed by Photoactivated Localization Microscopy
title_fullStr	Remodeling of the Z-Ring Nanostructure during the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Cell Cycle Revealed by Photoactivated Localization Microscopy
title_full_unstemmed	Remodeling of the Z-Ring Nanostructure during the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Cell Cycle Revealed by Photoactivated Localization Microscopy
title_sort	remodeling of the z-ring nanostructure during the <named-content content-type="genus-species">streptococcus pneumoniae</named-content> cell cycle revealed by photoactivated localization microscopy
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/853c889d41384c5d90b7073ad431744e
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Remodeling of the Z-Ring Nanostructure during the <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Cell Cycle Revealed by Photoactivated Localization Microscopy

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