A Polymerization-Associated Structural Switch in FtsZ That Enables Treadmilling of Model Filaments

ABSTRACT Bacterial cell division in many organisms involves a constricting cytokinetic ring that is orchestrated by the tubulin-like protein FtsZ. FtsZ forms dynamic filaments close to the membrane at the site of division that have recently been shown to treadmill around the division ring, guiding s...

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Autores principales:	James M. Wagstaff, Matthew Tsim, María A. Oliva, Alba García-Sanchez, Danguole Kureisaite-Ciziene, José Manuel Andreu, Jan Löwe
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/7244a9892d25432fa3aa02495ef6f826
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spelling	oai:doaj.org-article:7244a9892d25432fa3aa02495ef6f8262021-11-15T15:51:29ZA Polymerization-Associated Structural Switch in FtsZ That Enables Treadmilling of Model Filaments10.1128/mBio.00254-172150-7511https://doaj.org/article/7244a9892d25432fa3aa02495ef6f8262017-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00254-17https://doaj.org/toc/2150-7511ABSTRACT Bacterial cell division in many organisms involves a constricting cytokinetic ring that is orchestrated by the tubulin-like protein FtsZ. FtsZ forms dynamic filaments close to the membrane at the site of division that have recently been shown to treadmill around the division ring, guiding septal wall synthesis. Here, using X-ray crystallography of Staphylococcus aureus FtsZ (SaFtsZ), we reveal how an FtsZ can adopt two functionally distinct conformations, open and closed. The open form is found in SaFtsZ filaments formed in crystals and also in soluble filaments of Escherichia coli FtsZ as deduced by electron cryomicroscopy. The closed form is found within several crystal forms of two nonpolymerizing SaFtsZ mutants and corresponds to many previous FtsZ structures from other organisms. We argue that FtsZ’s conformational switch is polymerization-associated, driven by the formation of the longitudinal intersubunit interfaces along the filament. We show that such a switch provides explanations for both how treadmilling may occur within a single-stranded filament and why filament assembly is cooperative. IMPORTANCE The FtsZ protein is a key molecule during bacterial cell division. FtsZ forms filaments that organize cell membrane constriction, as well as remodeling of the cell wall, to divide cells. FtsZ functions through nucleotide-driven filament dynamics that are poorly understood at the molecular level. In particular, mechanisms for cooperative assembly (nonlinear dependency on concentration) and treadmilling (preferential growth at one filament end and loss at the other) have remained elusive. Here, we show that most likely all FtsZ proteins have two distinct conformations, a “closed” form in monomeric FtsZ and an “open” form in filaments. The conformational switch that occurs upon polymerization explains cooperativity and, in concert with polymerization-dependent nucleotide hydrolysis, efficient treadmilling of FtsZ polymers.James M. WagstaffMatthew TsimMaría A. OlivaAlba García-SanchezDanguole Kureisaite-CizieneJosé Manuel AndreuJan LöweAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 8, Iss 3 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 James M. Wagstaff Matthew Tsim María A. Oliva Alba García-Sanchez Danguole Kureisaite-Ciziene José Manuel Andreu Jan Löwe A Polymerization-Associated Structural Switch in FtsZ That Enables Treadmilling of Model Filaments
description	ABSTRACT Bacterial cell division in many organisms involves a constricting cytokinetic ring that is orchestrated by the tubulin-like protein FtsZ. FtsZ forms dynamic filaments close to the membrane at the site of division that have recently been shown to treadmill around the division ring, guiding septal wall synthesis. Here, using X-ray crystallography of Staphylococcus aureus FtsZ (SaFtsZ), we reveal how an FtsZ can adopt two functionally distinct conformations, open and closed. The open form is found in SaFtsZ filaments formed in crystals and also in soluble filaments of Escherichia coli FtsZ as deduced by electron cryomicroscopy. The closed form is found within several crystal forms of two nonpolymerizing SaFtsZ mutants and corresponds to many previous FtsZ structures from other organisms. We argue that FtsZ’s conformational switch is polymerization-associated, driven by the formation of the longitudinal intersubunit interfaces along the filament. We show that such a switch provides explanations for both how treadmilling may occur within a single-stranded filament and why filament assembly is cooperative. IMPORTANCE The FtsZ protein is a key molecule during bacterial cell division. FtsZ forms filaments that organize cell membrane constriction, as well as remodeling of the cell wall, to divide cells. FtsZ functions through nucleotide-driven filament dynamics that are poorly understood at the molecular level. In particular, mechanisms for cooperative assembly (nonlinear dependency on concentration) and treadmilling (preferential growth at one filament end and loss at the other) have remained elusive. Here, we show that most likely all FtsZ proteins have two distinct conformations, a “closed” form in monomeric FtsZ and an “open” form in filaments. The conformational switch that occurs upon polymerization explains cooperativity and, in concert with polymerization-dependent nucleotide hydrolysis, efficient treadmilling of FtsZ polymers.
format	article
author	James M. Wagstaff Matthew Tsim María A. Oliva Alba García-Sanchez Danguole Kureisaite-Ciziene José Manuel Andreu Jan Löwe
author_facet	James M. Wagstaff Matthew Tsim María A. Oliva Alba García-Sanchez Danguole Kureisaite-Ciziene José Manuel Andreu Jan Löwe
author_sort	James M. Wagstaff
title	A Polymerization-Associated Structural Switch in FtsZ That Enables Treadmilling of Model Filaments
title_short	A Polymerization-Associated Structural Switch in FtsZ That Enables Treadmilling of Model Filaments
title_full	A Polymerization-Associated Structural Switch in FtsZ That Enables Treadmilling of Model Filaments
title_fullStr	A Polymerization-Associated Structural Switch in FtsZ That Enables Treadmilling of Model Filaments
title_full_unstemmed	A Polymerization-Associated Structural Switch in FtsZ That Enables Treadmilling of Model Filaments
title_sort	polymerization-associated structural switch in ftsz that enables treadmilling of model filaments
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/7244a9892d25432fa3aa02495ef6f826
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A Polymerization-Associated Structural Switch in FtsZ That Enables Treadmilling of Model Filaments

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