Three-dimensional Macromolecular Organization of Cryofixed Myxococcus Xanthus Biofilms As Revealed by Electron Microscopic Tomography

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 2009 Jan 27

PMID 19168614

Citations 35

Authors

Hildur Palsdottir

Jonathan P Remis

Christoph Schaudinn

Eileen OToole

Renate Lux

Wenyuan Shi

Kent L McDonald

J William Costerton

Manfred Auer

Affiliations

Soon will be listed here.

Abstract

Despite the fact that most bacteria grow in biofilms in natural and pathogenic ecosystems, very little is known about the ultrastructure of their component cells or about the details of their community architecture. We used high-pressure freezing and freeze-substitution to minimize the artifacts of chemical fixation, sample aggregation, and sample extraction. As a further innovation we have, for the first time in biofilm research, used electron tomography and three-dimensional (3D) visualization to better resolve the macromolecular 3D ultrastructure of a biofilm. This combination of superb specimen preparation and greatly improved resolution in the z axis has opened a window in studies of Myxococcus xanthus cell ultrastructure and biofilm community architecture. New structural information on the chromatin body, cytoplasmic organization, membrane apposition between adjacent cells, and structure and distribution of pili and vesicles in the biofilm matrix is presented.

Citing Articles

OprF functions as a latch to direct Outer Membrane Vesicle release in .

Mathur S, Erickson S, Goldberg L, Hills S, Radin A, Schertzer J bioRxiv. 2023; .

PMID: 37986865 PMC: 10659412. DOI: 10.1101/2023.11.12.566662.

Outer Membrane Vesicle Vaccine Platforms.

Micoli F, Adamo R, Nakakana U BioDrugs. 2023; 38(1):47-59.

PMID: 37796436 PMC: 10789842. DOI: 10.1007/s40259-023-00627-0.

Membrane vesicles released by Lacticaseibacillus casei BL23 inhibit the biofilm formation of Salmonella Enteritidis.

da Silva Barreira D, Laurent J, Lourenco J, Ducassou J, Coute Y, Guzzo J Sci Rep. 2023; 13(1):1163.

PMID: 36670157 PMC: 9859808. DOI: 10.1038/s41598-023-27959-9.

Outer Membrane Vesicles: Biogenesis, Functions, and Issues.

Juodeikis R, Carding S Microbiol Mol Biol Rev. 2022; 86(4):e0003222.

PMID: 36154136 PMC: 9881588. DOI: 10.1128/mmbr.00032-22.

and outer membrane vesicles.

Yilmaz Colak C, Ozturk B Pathog Glob Health. 2022; 117(4):342-355.

PMID: 36047634 PMC: 10177744. DOI: 10.1080/20477724.2022.2117937.

References

Durrenberger M, Villiger W, Bachi T . Conjugational junctions: morphology of specific contacts in conjugating Escherichia coli bacteria. J Struct Biol. 1991; 107(2):146-56. DOI: 10.1016/1047-8477(91)90018-r. View

Fiocca R, Necchi V, Sommi P, Ricci V, Telford J, Cover T . Release of Helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles. Uptake of released toxin and vesicles by gastric epithelium. J Pathol. 1999; 188(2):220-6. DOI: 10.1002/(SICI)1096-9896(199906)188:2<220::AID-PATH307>3.0.CO;2-C. View

Mayrand D, Grenier D . Biological activities of outer membrane vesicles. Can J Microbiol. 1989; 35(6):607-13. DOI: 10.1139/m89-097. View

Hobot J, Villiger W, Escaig J, Maeder M, RYTER A, Kellenberger E . Shape and fine structure of nucleoids observed on sections of ultrarapidly frozen and cryosubstituted bacteria. J Bacteriol. 1985; 162(3):960-71. PMC: 215869. DOI: 10.1128/jb.162.3.960-971.1985. View

Mashburn L, Whiteley M . Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature. 2005; 437(7057):422-5. DOI: 10.1038/nature03925. View

Bajaj C, Yu Z, Auer M . Volumetric feature extraction and visualization of tomographic molecular imaging. J Struct Biol. 2003; 144(1-2):132-43. DOI: 10.1016/j.jsb.2003.09.037. View

McDonald K, Morphew M, Verkade P, Muller-Reichert T . Recent advances in high-pressure freezing: equipment- and specimen-loading methods. Methods Mol Biol. 2007; 369:143-73. DOI: 10.1007/978-1-59745-294-6_8. View

Ginsberg L, GERSHFELD N . Phospholipid surface bilayers at the air-water interface. II. Water permeability of dimyristoylphosphatidylcholine surface bilayers. Biophys J. 1985; 47(2 Pt 1):211-5. PMC: 1435153. DOI: 10.1016/s0006-3495(85)83893-5. View

Pelling A, Li Y, Shi W, Gimzewski J . Nanoscale visualization and characterization of Myxococcus xanthus cells with atomic force microscopy. Proc Natl Acad Sci U S A. 2005; 102(18):6484-9. PMC: 1088375. DOI: 10.1073/pnas.0501207102. View

10.

Lawrence J, Swerhone G, Leppard G, Araki T, Zhang X, West M . Scanning transmission X-ray, laser scanning, and transmission electron microscopy mapping of the exopolymeric matrix of microbial biofilms. Appl Environ Microbiol. 2003; 69(9):5543-54. PMC: 194976. DOI: 10.1128/AEM.69.9.5543-5554.2003. View

11.

Tajima K, GERSHFELD N . Phospholipid surface bilayers at the air-water interface. I. Thermodynamic properties. Biophys J. 1985; 47(2 Pt 1):203-9. PMC: 1435155. DOI: 10.1016/s0006-3495(85)83892-3. View

12.

Costerton J, Lewandowski Z, Caldwell D, Korber D, Lappin-Scott H . Microbial biofilms. Annu Rev Microbiol. 1995; 49:711-45. DOI: 10.1146/annurev.mi.49.100195.003431. View

13.

Stoodley P, Sauer K, Davies D, Costerton J . Biofilms as complex differentiated communities. Annu Rev Microbiol. 2002; 56:187-209. DOI: 10.1146/annurev.micro.56.012302.160705. View

14.

Schooling S, Beveridge T . Membrane vesicles: an overlooked component of the matrices of biofilms. J Bacteriol. 2006; 188(16):5945-57. PMC: 1540058. DOI: 10.1128/JB.00257-06. View

15.

Nudleman E, Wall D, Kaiser D . Cell-to-cell transfer of bacterial outer membrane lipoproteins. Science. 2005; 309(5731):125-7. DOI: 10.1126/science.1112440. View

16.

Curtis P, Atwood 3rd J, Orlando R, Shimkets L . Proteins associated with the Myxococcus xanthus extracellular matrix. J Bacteriol. 2007; 189(21):7634-42. PMC: 2168726. DOI: 10.1128/JB.01007-07. View

17.

Kadurugamuwa J, Beveridge T . Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J Bacteriol. 1995; 177(14):3998-4008. PMC: 177130. DOI: 10.1128/jb.177.14.3998-4008.1995. View

18.

Samuels A, LANKA E, Davies J . Conjugative junctions in RP4-mediated mating of Escherichia coli. J Bacteriol. 2000; 182(10):2709-15. PMC: 101974. DOI: 10.1128/JB.182.10.2709-2715.2000. View

19.

Hodgkin J, Kaiser D . Cell-to-cell stimulation of movement in nonmotile mutants of Myxococcus. Proc Natl Acad Sci U S A. 1977; 74(7):2938-42. PMC: 431354. DOI: 10.1073/pnas.74.7.2938. View

20.

Pettersen E, Goddard T, Huang C, Couch G, Greenblatt D, Meng E . UCSF Chimera--a visualization system for exploratory research and analysis. J Comput Chem. 2004; 25(13):1605-12. DOI: 10.1002/jcc.20084. View