Secondary bacterial flagellar system improves bacterial spreading by increasing the directional persistence of swimming
Sebastian Bubendorfera,b,c,1, Mihaly Koltaia,d,1, Florian Rossmanna,b, Victor Sourjika,d, and Kai M. Thormanna,b,2
aMax Planck Institute for Terrestrial Microbiology and LOEWE Research Center for Synthetic Microbiology (SYNMICRO), 35043 Marburg, Germany;
bInstitute for Microbiology and Molecular Biology, IFZ Interdisciplinary Research Centre, Justus Liebig University Giessen, 35392 Giessen, Germany;
cInstitute for Medical Microbiology and Hospital Epidemiology, Hannover Medical School, 30625 Hannover, Germany; and
dZentrum für Molekulare Biologie der Universität Heidelberg, DKFZ-ZMBH Alliance, 69120 Heidelberg, Germany
Edited by Caroline S. Harwood, University of Washington, Seattle, WA, and approved June 29, 2014 (received for review March 28, 2014)
Flagella-mediated motility is an important or even crucial propagation factor for many bacteria. A number of polarly flagellated species possess a distinct secondary flagellar system, which, as current models suggest, allows more effective swimming under conditions of elevated viscosity or across surfaces. In this study, we demonstrate that such a secondary flagellar system may also exert beneficial effects in bacterial spreading by increasing the directional persistence through lowering the cellular turning angles. The strategy of increasing directional persistence to improve animal spreading efficiency has been proposed previously by theoretical modeling, and here we provide a specific example of how this strategy is used by bacteria.
As numerous bacterial species, Shewanella putrefaciens CN-32 possesses a complete secondary flagellar system. A significant subpopulation of CN-32 cells induces expression of the secondary system under planktonic conditions, resulting in formation of one, sometimes two, filaments at lateral positions in addition to the primary polar flagellum. Mutant analysis revealed that the single chemotaxis system primarily or even exclusively addresses the main polar flagellar system. Cells with secondary filaments outperformed their monopolarly flagellated counterparts in spreading on soft-agar plates and through medium-filled channels despite having lower swimming speed. While mutant cells with only polar flagella navigate by a “run-reverse-flick” mechanism resulting in effective cell realignments of about 90°, wild-type cells with secondary filaments exhibited a range of realignment angles with an average value of smaller than 90°. Mathematical modeling and computer simulations demonstrated that the smaller realignment angle of wild-type cells results in the higher directional persistence, increasing spreading efficiency both with and without a chemical gradient. Taken together, we propose that in S. putrefaciens CN-32, cell propulsion and directional switches are mainly mediated by the polar flagellar system, while the secondary filament increases the directional persistence of swimming and thus of spreading in the environment.
bacterial motility cell reorientation CheY lateral flagella
1S.B. and M.K. contributed equally to this work.
2To whom correspondence should be addressed. Email: Kai.Thormann@mikro.bio.uni-giessen.de.
Author contributions: S.B., M.K., V.S., and K.M.T. designed research; S.B., M.K., and F.R. performed research; S.B., M.K., F.R., V.S., and K.M.T. analyzed data; and S.B., M.K., V.S., and K.M.T. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
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