FtsZ-Dependent Elongation of a Coccoid Bacterium

ABSTRACT A mechanistic understanding of the determination and maintenance of the simplest bacterial cell shape, a sphere, remains elusive compared with that of more complex shapes. Cocci seem to lack a dedicated elongation machinery, and a spherical shape has been considered an evolutionary dead-end...

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Autores principales:	Ana R. Pereira, Jen Hsin, Ewa Król, Andreia C. Tavares, Pierre Flores, Egbert Hoiczyk, Natalie Ng, Alex Dajkovic, Yves V. Brun, Michael S. VanNieuwenhze, Terry Roemer, Rut Carballido-Lopez, Dirk-Jan Scheffers, Kerwyn Casey Huang, Mariana G. Pinho
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f16c8280e23f43a6a894f35a18b85773
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spelling	oai:doaj.org-article:f16c8280e23f43a6a894f35a18b857732021-11-15T15:50:14ZFtsZ-Dependent Elongation of a Coccoid Bacterium10.1128/mBio.00908-162150-7511https://doaj.org/article/f16c8280e23f43a6a894f35a18b857732016-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00908-16https://doaj.org/toc/2150-7511ABSTRACT A mechanistic understanding of the determination and maintenance of the simplest bacterial cell shape, a sphere, remains elusive compared with that of more complex shapes. Cocci seem to lack a dedicated elongation machinery, and a spherical shape has been considered an evolutionary dead-end morphology, as a transition from a spherical to a rod-like shape has never been observed in bacteria. Here we show that a Staphylococcus aureus mutant (M5) expressing the ftsZG193D allele exhibits elongated cells. Molecular dynamics simulations and in vitro studies indicate that FtsZG193D filaments are more twisted and shorter than wild-type filaments. In vivo, M5 cell wall deposition is initiated asymmetrically, only on one side of the cell, and progresses into a helical pattern rather than into a constricting ring as in wild-type cells. This helical pattern of wall insertion leads to elongation, as in rod-shaped cells. Thus, structural flexibility of FtsZ filaments can result in an FtsZ-dependent mechanism for generating elongated cells from cocci. IMPORTANCE The mechanisms by which bacteria generate and maintain even the simplest cell shape remain an elusive but fundamental question in microbiology. In the absence of examples of coccus-to-rod transitions, the spherical shape has been suggested to be an evolutionary dead end in morphogenesis. We describe the first observation of the generation of elongated cells from truly spherical cocci, occurring in a Staphylococcus aureus mutant containing a single point mutation in its genome, in the gene encoding the bacterial tubulin homologue FtsZ. We demonstrate that FtsZ-dependent cell elongation is possible, even in the absence of dedicated elongation machinery.Ana R. PereiraJen HsinEwa KrólAndreia C. TavaresPierre FloresEgbert HoiczykNatalie NgAlex DajkovicYves V. BrunMichael S. VanNieuwenhzeTerry RoemerRut Carballido-LopezDirk-Jan ScheffersKerwyn Casey HuangMariana G. PinhoAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 5 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Ana R. Pereira Jen Hsin Ewa Król Andreia C. Tavares Pierre Flores Egbert Hoiczyk Natalie Ng Alex Dajkovic Yves V. Brun Michael S. VanNieuwenhze Terry Roemer Rut Carballido-Lopez Dirk-Jan Scheffers Kerwyn Casey Huang Mariana G. Pinho FtsZ-Dependent Elongation of a Coccoid Bacterium
description	ABSTRACT A mechanistic understanding of the determination and maintenance of the simplest bacterial cell shape, a sphere, remains elusive compared with that of more complex shapes. Cocci seem to lack a dedicated elongation machinery, and a spherical shape has been considered an evolutionary dead-end morphology, as a transition from a spherical to a rod-like shape has never been observed in bacteria. Here we show that a Staphylococcus aureus mutant (M5) expressing the ftsZG193D allele exhibits elongated cells. Molecular dynamics simulations and in vitro studies indicate that FtsZG193D filaments are more twisted and shorter than wild-type filaments. In vivo, M5 cell wall deposition is initiated asymmetrically, only on one side of the cell, and progresses into a helical pattern rather than into a constricting ring as in wild-type cells. This helical pattern of wall insertion leads to elongation, as in rod-shaped cells. Thus, structural flexibility of FtsZ filaments can result in an FtsZ-dependent mechanism for generating elongated cells from cocci. IMPORTANCE The mechanisms by which bacteria generate and maintain even the simplest cell shape remain an elusive but fundamental question in microbiology. In the absence of examples of coccus-to-rod transitions, the spherical shape has been suggested to be an evolutionary dead end in morphogenesis. We describe the first observation of the generation of elongated cells from truly spherical cocci, occurring in a Staphylococcus aureus mutant containing a single point mutation in its genome, in the gene encoding the bacterial tubulin homologue FtsZ. We demonstrate that FtsZ-dependent cell elongation is possible, even in the absence of dedicated elongation machinery.
format	article
author	Ana R. Pereira Jen Hsin Ewa Król Andreia C. Tavares Pierre Flores Egbert Hoiczyk Natalie Ng Alex Dajkovic Yves V. Brun Michael S. VanNieuwenhze Terry Roemer Rut Carballido-Lopez Dirk-Jan Scheffers Kerwyn Casey Huang Mariana G. Pinho
author_facet	Ana R. Pereira Jen Hsin Ewa Król Andreia C. Tavares Pierre Flores Egbert Hoiczyk Natalie Ng Alex Dajkovic Yves V. Brun Michael S. VanNieuwenhze Terry Roemer Rut Carballido-Lopez Dirk-Jan Scheffers Kerwyn Casey Huang Mariana G. Pinho
author_sort	Ana R. Pereira
title	FtsZ-Dependent Elongation of a Coccoid Bacterium
title_short	FtsZ-Dependent Elongation of a Coccoid Bacterium
title_full	FtsZ-Dependent Elongation of a Coccoid Bacterium
title_fullStr	FtsZ-Dependent Elongation of a Coccoid Bacterium
title_full_unstemmed	FtsZ-Dependent Elongation of a Coccoid Bacterium
title_sort	ftsz-dependent elongation of a coccoid bacterium
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/f16c8280e23f43a6a894f35a18b85773
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FtsZ-Dependent Elongation of a Coccoid Bacterium

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