DOI: 10.1128/jb.00957-07. Cell Surface Filaments of the Gliding Bacterium <i>Flavobacterium johnsoniae</i> Revealed by Cryo-Electron Tomography

Cell Surface Filaments of the Gliding Bacterium Flavobacterium johnsoniae Revealed by Cryo-Electron Tomography

10.1128/jb.00957-07

Crossref journal-article

American Society for Microbiology

Journal of Bacteriology (235)

Abstract

ABSTRACT Flavobacterium johnsoniae cells glide rapidly over surfaces by an as-yet-unknown mechanism. Using cryo-electron tomography, we show that wild-type cells display tufts of ∼5-nm-wide cell surface filaments that appear to be anchored to the inner surface of the outer membrane. These filaments are absent in cells of a nonmotile gldF mutant but are restored upon expression of plasmid-encoded GldF, a component of a putative ATP-binding cassette transporter.

Bibliography

Liu, J., McBride, M. J., & Subramaniam, S. (2007). Cell Surface Filaments of the Gliding Bacterium Flavobacterium johnsoniae Revealed by Cryo-Electron Tomography. Journal of Bacteriology, 189(20), 7503â7506.

Authors 3

Jun Liu (first)
Mark J. McBride (additional)
Sriram Subramaniam (additional)

References 25 Referenced 65

Abbanat, D. R., E. R. Leadbetter, W. Godchaux III, and A. Escher. 1986. Sulphonolipids are molecular determinants of gliding motility. Nature 324 : 367-369. (10.1038/324367a0) / Nature (1986)
Agarwal, S., D. W. Hunnicutt, and M. J. McBride. 1997. Cloning and characterization of the Flavobacterium johnsoniae (Cytophaga johnsonae) gliding motility gene, gldA. Proc. Natl. Acad. Sci. USA 94 : 12139-12144. (10.1073/pnas.94.22.12139) / Proc. Natl. Acad. Sci. USA (1997)
Beatson, P. J., and K. C. Marshall. 1994. A proposed helical mechanism for gliding motility in three gliding bacteria (order Cytophagales). Can. J. Microbiol. 40 : 173-183. (10.1139/m94-030) / Can. J. Microbiol. (1994)
10.1128/JB.187.20.6943-6952.2005
10.1128/JB.187.8.2628-2637.2005
Burchard, R. P. 1981. Gliding motility of prokaryotes: ultrastructure, physiology, and genetics. Annu. Rev. Microbiol. 35 : 497-529. (10.1146/annurev.mi.35.100181.002433) / Annu. Rev. Microbiol. (1981)
10.1128/jb.173.23.7607-7614.1991
10.1128/JB.184.9.2370-2378.2002
10.1128/JB.183.14.4167-4175.2001
10.1128/JB.182.4.911-918.2000
10.1128/jb.151.1.384-398.1982
10.1146/annurev.micro.55.1.49
McBride, M. J. 2004. Cytophaga-flavobacterium gliding motility. J. Mol. Microbiol. Biotechnol. 7 : 63-71. (10.1159/000077870) / J. Mol. Microbiol. Biotechnol. (2004)
10.1128/JB.186.8.2295-2302.2004
10.1128/JB.185.22.6648-6657.2003
Pate, J. L. 1985. Gliding motility in Cytophaga. Microbiol. Sci. 2 : 289-295. / Microbiol. Sci. (1985)
Pate, J. L. 1988. Gliding motility in procaryotic cells. Can. J. Microbiol. 34 : 459-465. (10.1139/m88-079) / Can. J. Microbiol. (1988)
Pate, J. L., and L.-Y. E. Chang. 1979. Evidence that gliding motility in prokaryotic cells is driven by rotary assemblies in the cell envelopes. Curr. Microbiol. 2 : 59-64. (10.1007/BF02601737) / Curr. Microbiol. (1979)
Ridgway, H. F., and R. A. Lewin. 1988. Characterization of gliding motility in Flexibacter polymorphus. Cell Motil. Cytoskelet. 11 : 46-63. (10.1002/cm.970110106) / Cell Motil. Cytoskelet. (1988)
Samuel, A. D., J. D. Petersen, and T. S. Reese. 2001. Envelope structure of Synechococcus sp. WH8113, a nonflagellated swimming cyanobacterium. BMC Microbiol. 1 : 4. (10.1186/1471-2180-1-4) / BMC Microbiol. (2001)
Subramaniam, S. 2005. Bridging the imaging gap: visualizing subcellular architecture with electron tomography. Curr. Opin. Microbiol. 8 : 316-322. (10.1016/j.mib.2005.04.012) / Curr. Opin. Microbiol. (2005)
Winkler, H., and K. A. Taylor. 2006. Accurate marker-free alignment with simultaneous geometry determination and reconstruction of tilt series in electron tomography. Ultramicroscopy 106 : 240-254. (10.1016/j.ultramic.2005.07.007) / Ultramicroscopy (2006)
10.1128/AEM.00225-07
Zhang, P., E. Bos, J. Heymann, H. Gnaegi, M. Kessel, P. J. Peters, and S. Subramaniam. 2004. Direct visualization of receptor arrays in frozen-hydrated sections and plunge-frozen specimens of E. coli engineered to overproduce the chemotaxis receptor Tsr. J. Microsc. 216 : 76-83. (10.1111/j.0022-2720.2004.01395.x) / J. Microsc. (2004)
Zhang, P., C. M. Khursigara, L. M. Hartnell, and S. Subramaniam. 2007. Direct visualization of Escherichia coli chemotaxis receptor arrays using cryo-electron microscopy. Proc. Natl. Acad. Sci. USA 104 : 3777-3781. (10.1073/pnas.0610106104) / Proc. Natl. Acad. Sci. USA (2007)

Dates

Type	When
Created	18 years ago (Aug. 10, 2007, 9 p.m.)
Deposited	4 years, 1 month ago (July 29, 2021, 1:36 p.m.)
Indexed	3 months ago (May 26, 2025, 5:06 a.m.)
Issued	17 years, 10 months ago (Oct. 15, 2007)
Published	17 years, 10 months ago (Oct. 15, 2007)
Published Print	17 years, 10 months ago (Oct. 15, 2007)

Funders 0

None

BibTeX

@article{Liu_2007, title={Cell Surface Filaments of the Gliding Bacterium Flavobacterium johnsoniae Revealed by Cryo-Electron Tomography}, volume={189}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.00957-07}, DOI={10.1128/jb.00957-07}, number={20}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Liu, Jun and McBride, Mark J. and Subramaniam, Sriram}, year={2007}, month=oct, pages={7503–7506} }

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