Abstract
The cell walls of four gliding filamentous Oscillatoriaceae species comprising three different genera were studied by freeze substitution, freeze fracturing, and negative staining. In all species, the multilayered gram-negative cell wall is covered with a complex external double layer. The first layer is a tetragonal crystalline S-layer anchored on the outer membrane. The second array is formed by parallel, helically arranged surface fibrils with diameters of 8 to 12 nm. These fibrils have a serrated appearance in cross sections. In all cases, the orientation of the surface fibrils correlates with the sense of revolution of the filaments during gliding, i.e., clockwise in both Phormidium strains and counterclockwise in Oscillatoria princeps and Lyngbya aeruginosa. The lack of longitudinal corrugations or contractions of the surface fibrils and the identical appearances of motile and nonmotile filaments suggest that this structure plays a passive screw thread role in gliding. It is hypothesized that the necessary propulsive force is generated by shear forces between the surface fibrils and the continuing flow of secreted extracellular slime. Furthermore, the so-called junctional pores seem to be the extrusion sites of the slime. In motile cells, these pores exhibit a different staining behavior than that seen in nonmotile ones. In the former, the channels of the pores are filled with electron-dense material, whereas in the latter, the channels appear comparatively empty, highly contrasting the peptidoglycan. Finally, the presence of regular surface structures in other gliding prokaryotes is considered an indication that comparable structures are general features of the cell walls of gliding microbes.
Full Text
The Full Text of this article is available as a PDF (2.7 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Brown R. M., Jr, Willison J. H., Richardson C. L. Cellulose biosynthesis in Acetobacter xylinum: visualization of the site of synthesis and direct measurement of the in vivo process. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4565–4569. doi: 10.1073/pnas.73.12.4565. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burchard A. C., Burchard R. P., Kloetzel J. A. Intracellular, periodic structures in the gliding bacterium Myxococcus xanthus. J Bacteriol. 1977 Nov;132(2):666–672. doi: 10.1128/jb.132.2.666-672.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burchard R. P. Gliding motility of prokaryotes: ultrastructure, physiology, and genetics. Annu Rev Microbiol. 1981;35:497–529. doi: 10.1146/annurev.mi.35.100181.002433. [DOI] [PubMed] [Google Scholar]
- Castenholz R. W. Thermophilic blue-green algae and the thermal environment. Bacteriol Rev. 1969 Dec;33(4):476–504. doi: 10.1128/br.33.4.476-504.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dworkin M. Biology of the myxobacteria. Annu Rev Microbiol. 1966;20:75–106. doi: 10.1146/annurev.mi.20.100166.000451. [DOI] [PubMed] [Google Scholar]
- Dworkin M., Keller K. H., Weisberg D. Experimental observations consistent with a surface tension model of gliding motility of Myxococcus xanthus. J Bacteriol. 1983 Sep;155(3):1367–1371. doi: 10.1128/jb.155.3.1367-1371.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fattom A., Shilo M. Hydrophobicity as an adhesion mechanism of benthic cyanobacteria. Appl Environ Microbiol. 1984 Jan;47(1):135–143. doi: 10.1128/aem.47.1.135-143.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Golecki J. R. Studies on ultrastructure and composition of cell walls of the cyanobacterium Anacystis nidulans. Arch Microbiol. 1977 Jul 26;114(1):35–41. doi: 10.1007/BF00429627. [DOI] [PubMed] [Google Scholar]
- Graham L. L., Beveridge T. J. Effect of chemical fixatives on accurate preservation of Escherichia coli and Bacillus subtilis structure in cells prepared by freeze-substitution. J Bacteriol. 1990 Apr;172(4):2150–2159. doi: 10.1128/jb.172.4.2150-2159.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Graham L. L. Freeze-substitution studies of bacteria. Electron Microsc Rev. 1992;5(1):77–103. doi: 10.1016/0892-0354(92)90006-c. [DOI] [PubMed] [Google Scholar]
- Graham L. L., Harris R., Villiger W., Beveridge T. J. Freeze-substitution of gram-negative eubacteria: general cell morphology and envelope profiles. J Bacteriol. 1991 Mar;173(5):1623–1633. doi: 10.1128/jb.173.5.1623-1633.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hobot J. A., Carlemalm E., Villiger W., Kellenberger E. Periplasmic gel: new concept resulting from the reinvestigation of bacterial cell envelope ultrastructure by new methods. J Bacteriol. 1984 Oct;160(1):143–152. doi: 10.1128/jb.160.1.143-152.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lamont H. C. Shear-oriented microfibrils in the mucilaginous investments of two motile oscillatoriacean blue-green algae. J Bacteriol. 1969 Jan;97(1):350–361. doi: 10.1128/jb.97.1.350-361.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lapidus I. R., Berg H. C. Gliding motility of Cytophaga sp. strain U67. J Bacteriol. 1982 Jul;151(1):384–398. doi: 10.1128/jb.151.1.384-398.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Luft J. H. Ruthenium red and violet. I. Chemistry, purification, methods of use for electron microscopy and mechanism of action. Anat Rec. 1971 Nov;171(3):347–368. doi: 10.1002/ar.1091710302. [DOI] [PubMed] [Google Scholar]
- MacRae T. H., McCurdy D. Evidence for motility-related fimbriae in the gliding microorganism Myxococcus xanthus. Can J Microbiol. 1976 Oct;22(10):1589–1593. doi: 10.1139/m76-234. [DOI] [PubMed] [Google Scholar]
- Macalister T. J., Macdonald B., Rothfield L. I. The periseptal annulus: An organelle associated with cell division in Gram-negative bacteria. Proc Natl Acad Sci U S A. 1983 Mar;80(5):1372–1376. doi: 10.1073/pnas.80.5.1372. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maier S., Murray R. G. The fine structure of Thioploca ingrica and a comparison with Beggiatoa. Can J Microbiol. 1965 Aug;11(4):645–655. doi: 10.1139/m65-087. [DOI] [PubMed] [Google Scholar]
- PRINGSHEIM E. G. The Vitreoscillaceae; a family of colourless, gliding, filamentous organisms. J Gen Microbiol. 1951 Feb;5(1):124–149. doi: 10.1099/00221287-5-1-124. [DOI] [PubMed] [Google Scholar]
- REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reichenbach H., Golecki J. R. The fine structure of Herpetosiphon, and a note on the taxonomy of the genus. Arch Microbiol. 1975 Mar 10;102(3):281–291. doi: 10.1007/BF00428379. [DOI] [PubMed] [Google Scholar]
- Ridgway H. F., Wagner R. M., Dawsey W. T., Lewin R. A. Fine structure of the cell envelope layers of Flexibacter polymorphus. Can J Microbiol. 1975 Nov;21(11):1733–1750. doi: 10.1139/m75-254. [DOI] [PubMed] [Google Scholar]
- SCHULZ G. Bewegungsstudien sowie elektronenmikroskopische Membranuntersuchungen an Cyanophyceen. Arch Mikrobiol. 1955;21(4):335–370. [PubMed] [Google Scholar]
- Sleytr U. B., Messner P. Crystalline surface layers on bacteria. Annu Rev Microbiol. 1983;37:311–339. doi: 10.1146/annurev.mi.37.100183.001523. [DOI] [PubMed] [Google Scholar]
- Zaar K. Visualization of pores (export sites) correlated with cellulose production in the envelope of the gram-negative bacterium Acetobacter xylinum. J Cell Biol. 1979 Mar;80(3):773–777. doi: 10.1083/jcb.80.3.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van Eykelenburg C. On the morphology and ultrastructure of the cell wall of Spirulina platensis. Antonie Van Leeuwenhoek. 1977;43(2):89–99. doi: 10.1007/BF00395664. [DOI] [PubMed] [Google Scholar]