Biogenesis of actin-like bacterial cytoskeletal filaments destined for positioning prokaryotic magnetic organelles

doi:10.1073/pnas.0603760103

Biogenesis of actin-like bacterial cytoskeletal filaments destined for positioning prokaryotic magnetic organelles

*Laboratoire de Chimie Bactérienne Unité Propre de Recherche 9043 and
^†Service de Microscopie Electronique, Institut de Biologie Structurale et Microbiologie, Centre National de la Recherche Scientifique, 13402 Marseille, France; and
^‡Department of Life Science, Graduate School of Natural Science and Technology, Kanazawa University, Kanazawa 920, Japan

Edited by David J. DeRosier, Brandeis University, Waltham, MA, and approved September 23, 2006 (received for review May 8, 2006)

Abstract

Magnetosomes comprise a magnetic nanocrystal surrounded by a lipid bilayer membrane. These unique prokaryotic organelles align inside magnetotactic bacterial cells and serve as an intracellular compass allowing the bacteria to navigate along the geomagnetic field in aquatic environments. Cryoelectron tomography of Magnetospirillum strains has revealed that the magnetosome chain is surrounded by a network of filaments that may be composed of MamK given that the filaments are absent in the mamK mutant cells. The process of the MamK filament assembly is unknown. Here we prove the authenticity of the MamK filaments and show that MamK exhibits linear distribution inside Magnetospirillum sp. cells even in the area without magnetosomes. The mamK gene alone is sufficient to direct the synthesis of straight filaments in Escherichia coli, and one extremity of the MamK filaments is located at the cellular pole. By using dual fluorescent labeling of MamK, we found that MamK nucleates at multiple sites and assembles into mosaic filaments. Time-lapse experiments reveal that the assembly of the MamK filaments is a highly dynamic and kinetically asymmetrical process. MamK bundles might initiate the formation of a new filament or associate to one preexistent filament. Our results demonstrate the mechanism of biogenesis of prokaryotic cytoskeletal filaments that are structurally and functionally distinct from the known MreB and ParM filaments. In addition to positioning magnetosomes, other hypothetical functions of the MamK filaments in magnetotaxis might include anchoring magnetosomes and being involved in magnetic reception.

Footnotes

^§To whom correspondence should be addressed at:
Laboratoire de Chimie Bactérienne Unité Propre de Recherche 9043, Institut de Biologie Structurale et Microbiologie, Centre National de la Recherche Scientifique, 31 chemin Joseph Aiguier, 13402 Marseille Cedex 20, France.
E-mail: wu{at}ibsm.cnrs-mrs.fr
Author contributions: N.P., C.-L.S., A.B., and L.-F.W. designed research; N.P., C.-L.S., and A.B. performed research; Y.F. contributed new reagents/analytic tools; N.P., C.-L.S., A.B., and L.-F.W. analyzed data; and N.P. and L.-F.W. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS direct submission.
Abbreviations:

Amp,

ampicillin;

Cm,

chloramphenicol;

IPTG,

isopropyl β-d-thiogalactoside;

YFP,

yellow fluorescent protein.