FtsZ-Dependent Elongation of a Coccoid Bacterium

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 morpholo...

Full description

Bibliographic Details
Main Authors: 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
Format: Article
Language:English
Published: American Society for Microbiology 2016-09-01
Series:mBio
Online Access:http://mbio.asm.org/cgi/content/full/7/5/e00908-16
id doaj-07c6d0a930ed4683b0705f8171eb1e3e
record_format Article
spelling doaj-07c6d0a930ed4683b0705f8171eb1e3e2021-07-02T02:03:18ZengAmerican Society for MicrobiologymBio2150-75112016-09-0175e00908-1610.1128/mBio.00908-16FtsZ-Dependent Elongation of a Coccoid BacteriumAna R. PereiraJen HsinEwa KrólAndreia C. TavaresPierre FloresEgbert HoiczykNatalie NgAlex DajkovicYves V. BrunMichael S. VanNieuwenhzeTerry RoemerRut Carballido-LopezDirk-Jan ScheffersKerwyn Casey HuangMariana G. PinhoA 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.http://mbio.asm.org/cgi/content/full/7/5/e00908-16
collection DOAJ
language English
format Article
sources DOAJ
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
spellingShingle 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
mBio
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
series mBio
issn 2150-7511
publishDate 2016-09-01
description 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.
url http://mbio.asm.org/cgi/content/full/7/5/e00908-16
work_keys_str_mv AT anarpereira ftszdependentelongationofacoccoidbacterium
AT jenhsin ftszdependentelongationofacoccoidbacterium
AT ewakrol ftszdependentelongationofacoccoidbacterium
AT andreiactavares ftszdependentelongationofacoccoidbacterium
AT pierreflores ftszdependentelongationofacoccoidbacterium
AT egberthoiczyk ftszdependentelongationofacoccoidbacterium
AT natalieng ftszdependentelongationofacoccoidbacterium
AT alexdajkovic ftszdependentelongationofacoccoidbacterium
AT yvesvbrun ftszdependentelongationofacoccoidbacterium
AT michaelsvannieuwenhze ftszdependentelongationofacoccoidbacterium
AT terryroemer ftszdependentelongationofacoccoidbacterium
AT rutcarballidolopez ftszdependentelongationofacoccoidbacterium
AT dirkjanscheffers ftszdependentelongationofacoccoidbacterium
AT kerwyncaseyhuang ftszdependentelongationofacoccoidbacterium
AT marianagpinho ftszdependentelongationofacoccoidbacterium
_version_ 1721343897340215296