Hook length of the bacterial flagellum is optimized for maximal stability of the flagellar bundle

Spöring, Imke; Martinez, Vincent A.; Hotz, Christian; Schwarz-Linek, Jana; Grady, Keara L.; Nava-Sedeño, Josué M.; Vissers, Teun; Singer, Hanna M.; Rohde, Manfred; Bourquin, Carole; Hatzikirou, Haralampos; Poon, Wilson C. K.; Dufour, Yann S.; Erhardt, Marc

doi:10.1371/journal.pbio.2006989

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Hook length of the bacterial flagellum is optimized for maximal stability of the flagellar bundle

Spöring, Imke Institute for Biology and Bacterial Physiology, Humboldt-Universität zu Berlin, Berlin, Germany - Junior Research Group Infection Biology of Salmonella, Helmholtz Centre for Infection Research, Braunschweig, Germany
Martinez, Vincent A. School of Physics and Astronomy, The University of Edinburgh, Edinburgh, UK
Hotz, Christian Department of Medicine, Pharmacology, University of Fribourg, Switzerland,
Schwarz-Linek, Jana School of Physics and Astronomy, The University of Edinburgh, Edinburgh, UK
Grady, Keara L. Microbiology and Molecular Genetics, Michigan State University, East Lansing, USA
Nava-Sedeño, Josué M. Braunschweig Integrated Centre of Systems Biology (BRICS), Braunschweig, Germany
Vissers, Teun School of Physics and Astronomy, The University of Edinburgh, Edinburgh, UK
Singer, Hanna M. Department of Medicine, Microbiologie, University of Fribourg, Switzerland
Rohde, Manfred Central Facility for Microscopy, Helmholtz Centre for Infection Research, Braunschweig, Germany
Bourquin, Carole Department of Medicine, Pharmacology, University of Fribourg, Switzerland, - School of Pharmaceutical Sciences, University of Geneva, Switzerland
Hatzikirou, Haralampos Braunschweig Integrated Centre of Systems Biology (BRICS), Braunschweig, Germany - Systems Immunology, Helmholtz Centre for Infection Research, Braunschweig, Germany
Poon, Wilson C. K. School of Physics and Astronomy, The University of Edinburgh, Edinburgh, UK
Dufour, Yann S. Microbiology and Molecular Genetics, Michigan State University, East Lansing, USA
Erhardt, Marc Institute for Biology and Bacterial Physiology, Humboldt-Universität zu Berlin, Berlin, Germany - Junior Research Group Infection Biology of Salmonella, Helmholtz Centre for Infection Research, Braunschweig, Germany - Department of Medicine, Microbiologie, University of Fribourg, Switzerland

06.09.2018

Published in:

PLOS Biology. - 2018, vol. 16, no. 9, p. e2006989

English Most bacteria swim in liquid environments by rotating one or several flagella. The long external filament of the flagellum is connected to a membrane-embedded basal body by a flexible universal joint, the hook, which allows the transmission of motor torque to the filament. The length of the hook is controlled on a nanometer scale by a sophisticated molecular ruler mechanism. However, why its length is stringently controlled has remained elusive. We engineered and studied a diverse set of hook- length variants of Salmonella enterica. Measurements of plate-assay motility, single- cell swimming speed, and directional persistence in quasi-2D and population- averaged swimming speed and body angular velocity in 3D revealed that the motility performance is optimal around the wild-type hook length. We conclude that too-short hooks may be too stiff to function as a junction and too-long hooks may buckle and create instability in the flagellar bundle. Accordingly, peritrichously flagellated bacteria move most efficiently as the distance travelled per body rotation is maximal and body wobbling is minimized. Thus, our results suggest that the molecular ruler mechanism evolved to control flagellar hook growth to the optimal length consistent with efficient bundle formation. The hook-length control mechanism is therefore a prime example of how bacteria evolved elegant but robust mechanisms to maximize their fitness under specific environmental constraints.

Faculty

Faculté des sciences et de médecine

Department

Département de Médecine

Language