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Research Article

Bacteria exploit a polymorphic instability of the flagellar filament to escape from traps

Marco J. Kühn, Felix K. Schmidt, Bruno Eckhardt, and Kai M. Thormann
  1. aInstitut für Mikrobiologie und Molekularbiologie, Justus-Liebig-Universität Giessen, 35392 Giessen, Germany;
  2. bFachbereich Physik, Philipps-Universität Marburg, 35032 Marburg, Germany;
  3. cLOEWE Zentrum für Synthetische Mikrobiologie, Philipps-Universität Marburg, 35032 Marburg, Germany

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PNAS June 13, 2017 114 (24) 6340-6345; first published May 30, 2017; https://doi.org/10.1073/pnas.1701644114
Marco J. Kühn
aInstitut für Mikrobiologie und Molekularbiologie, Justus-Liebig-Universität Giessen, 35392 Giessen, Germany;
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Felix K. Schmidt
bFachbereich Physik, Philipps-Universität Marburg, 35032 Marburg, Germany;
cLOEWE Zentrum für Synthetische Mikrobiologie, Philipps-Universität Marburg, 35032 Marburg, Germany
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Bruno Eckhardt
bFachbereich Physik, Philipps-Universität Marburg, 35032 Marburg, Germany;
cLOEWE Zentrum für Synthetische Mikrobiologie, Philipps-Universität Marburg, 35032 Marburg, Germany
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Kai M. Thormann
aInstitut für Mikrobiologie und Molekularbiologie, Justus-Liebig-Universität Giessen, 35392 Giessen, Germany;
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  • For correspondence: kai.thormann@mikro.bio.uni-giessen.de
  1. Edited by Howard C. Berg, Harvard University, Cambridge, MA, and approved May 10, 2017 (received for review January 30, 2017)

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Significance

It has long been established that flagella provide an efficient means of movement for bacteria in planktonic environments (free swimming) or across surfaces (swarming). However, rather little is known about bacterial motility in structured environments. In this study, we demonstrate that polarly flagellated bacteria can exploit a polymorphic instability of the flagellar filament for a third type of flagella-mediated movement in which the flagellum wraps around the cell body and the cells back out from narrow passages in a screw-like motion.

Abstract

Many bacterial species swim by rotating single polar helical flagella. Depending on the direction of rotation, they can swim forward or backward and change directions to move along chemical gradients but also to navigate their obstructed natural environment in soils, sediments, or mucus. When they get stuck, they naturally try to back out, but they can also resort to a radically different flagellar mode, which we discovered here. Using high-speed microscopy, we monitored the swimming behavior of the monopolarly flagellated species Shewanella putrefaciens with fluorescently labeled flagellar filaments at an agarose–glass interface. We show that, when a cell gets stuck, the polar flagellar filament executes a polymorphic change into a spiral-like form that wraps around the cell body in a spiral-like fashion and enables the cell to escape by a screw-like backward motion. Microscopy and modeling suggest that this propagation mode is triggered by an instability of the flagellum under reversal of the rotation and the applied torque. The switch is reversible and bacteria that have escaped the trap can return to their normal swimming mode by another reversal of motor direction. The screw-type flagellar arrangement enables a unique mode of propagation and, given the large number of polarly flagellated bacteria, we expect it to be a common and widespread escape or motility mode in complex and structured environments.

  • Shewanella
  • flagella
  • motility
  • structured environment

Footnotes

  • ↵1To whom correspondence should be addressed. Email: kai.thormann{at}mikro.bio.uni-giessen.de.
  • Author contributions: M.J.K., F.K.S., B.E., and K.M.T. designed research; M.J.K. and F.K.S. performed research; M.J.K., F.K.S., B.E., and K.M.T. analyzed data; and M.J.K., F.K.S., B.E., and K.M.T. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1701644114/-/DCSupplemental.

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Flagella-mediated screwing by bacteria
Marco J. Kühn, Felix K. Schmidt, Bruno Eckhardt, Kai M. Thormann
Proceedings of the National Academy of Sciences Jun 2017, 114 (24) 6340-6345; DOI: 10.1073/pnas.1701644114

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Flagella-mediated screwing by bacteria
Marco J. Kühn, Felix K. Schmidt, Bruno Eckhardt, Kai M. Thormann
Proceedings of the National Academy of Sciences Jun 2017, 114 (24) 6340-6345; DOI: 10.1073/pnas.1701644114
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Proceedings of the National Academy of Sciences: 114 (24)
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