FtsZ-Dependent Elongation of a Coccoid Bacterium

Author:

Pereira Ana R.1,Hsin Jen2,Król Ewa3,Tavares Andreia C.1,Flores Pierre4,Hoiczyk Egbert56,Ng Natalie2,Dajkovic Alex4,Brun Yves V.7,VanNieuwenhze Michael S.8,Roemer Terry9,Carballido-Lopez Rut4,Scheffers Dirk-Jan3ORCID,Huang Kerwyn Casey210,Pinho Mariana G.1

Affiliation:

1. Bacterial Cell Biology, Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Oeiras, Portugal

2. Department of Bioengineering, Stanford University, Stanford, California, USA

3. Department of Molecular Microbiology, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Groningen, The Netherlands

4. MICALIS, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, France

5. W. Harry Feinstone Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA

6. Department of Molecular Biology and Biotechnology, The Krebs Institute, University of Sheffield, Sheffield, United Kingdom

7. Department of Biology, Indiana University, Bloomington, Indiana, USA

8. Department of Chemistry, Indiana University, Bloomington, Indiana, USA

9. Infectious Disease Research, Merck Research Laboratories, Kenilworth, New Jersey, USA

10. Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, California, USA

Abstract

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 ftsZ G193D allele exhibits elongated cells. Molecular dynamics simulations and in vitro studies indicate that FtsZ G193D 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.

Funder

Fundação para a Ciência e Tecnologia

Netherlands Organization for Scientific Reasearch

HHS | National Institutes of Health

EC | European Research Council

Agence Nationale de la Recherche

Publisher

American Society for Microbiology

Subject

Virology,Microbiology

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