Abstract
FtsZ is the major cytoskeletal component of the bacterial cell division machinery. It forms a ring-shaped structure (the Z ring) that constricts as the bacterium divides. Previous in vivo experiments with green fluorescent protein-labeled FtsZ and fluorescence recovery after photobleaching have shown that the Escherichia coli Z ring is extremely dynamic, continually remodeling itself with a half time of 30 s, similar to microtubules in the mitotic spindle. In the present work, under different experimental conditions, we have found that the half time for fluorescence recovery of E. coli Z rings is even shorter (approximately 9 s). As before, the turnover appears to be coupled to GTP hydrolysis, since the mutant FtsZ84 protein, with reduced GTPase in vitro, showed an approximately 3-fold longer half time. We have also extended the studies to Bacillus subtilis and found that this species exhibits equally rapid dynamics of the Z ring (half time, approximately 8 s). Interestingly, null mutations of the FtsZ-regulating proteins ZapA, EzrA, and MinCD had only modest effects on the assembly dynamics. This suggests that these proteins do not directly regulate FtsZ subunit exchange in and out of polymers. In B. subtilis, only 30 to 35% of the FtsZ protein was in the Z ring, from which we conclude that a Z ring only 2 or 3 protofilaments thick can function for cell division.
MeSH Terms
Adenosine Triphosphatases/genetics,metabolism
Artificial Gene Fusion
Bacillus subtilis/metabolism
Bacterial Proteins/genetics,metabolism
Cell Division/physiology
Cytoskeletal Proteins/metabolism
Escherichia coli/metabolism
Escherichia coli Proteins/genetics,metabolism
Fluorescence
GTP Phosphohydrolases/metabolism
Gene Deletion
Genes, Bacterial
Genes, Reporter
Green Fluorescent Proteins
Guanosine Triphosphate/metabolism
Half-Life
Luminescent Proteins/analysis,genetics,metabolism
Membrane Proteins/genetics,metabolism
Mutation
Chemicals
Bacterial Proteins
Cytoskeletal Proteins
Escherichia coli Proteins
EzrA protein, Bacillus subtilis
FtsZ protein, Bacteria
FtsZ84 protein, E coli
Luminescent Proteins
Membrane Proteins
MinC protein, Bacteria
MinC protein, E coli
Green Fluorescent Proteins
Guanosine Triphosphate
Adenosine Triphosphatases
GTP Phosphohydrolases
MinD protein, E coli
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Anderson David E
Department of Cell Biology, Duke University Medical Center, Durham, North Carolina 27710, USA.
Gueiros-Filho Frederico J
Erickson Harold P
References (30)
30 references, click to expand
-
Kinetics of protein-protein association explained by Brownian dynamics computer simulation.
Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3338-42
PMID: 1565624
-
Dynamic instability of microtubules.
Bioessays. 1987 Oct;7(4):149-54
PMID: 3318820
-
Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein.
Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):1053-7
PMID: 8430073
-
The FtsZ protein of Bacillus subtilis is localized at the division site and has GTPase activity that is dependent upon FtsZ concentration.
Mol Microbiol. 1993 Aug;9(3):435-42
PMID: 8412693
-
Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers.
Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):519-23
PMID: 8552673
-
Structure of the alpha beta tubulin dimer by electron crystallography.
Nature. 1998 Jan 8;391(6663):199-203
PMID: 9428769
-
Crystal structure of the bacterial cell-division protein FtsZ.
Nature. 1998 Jan 8;391(6663):203-6
PMID: 9428770
-
Microtubule polymerization dynamics.
Annu Rev Cell Dev Biol. 1997;13:83-117
PMID: 9442869
-
FtsZ from Escherichia coli, Azotobacter vinelandii, and Thermotoga maritima--quantitation, GTP hydrolysis, and assembly.
Cell Motil Cytoskeleton. 1998;40(1):71-86
PMID: 9605973
-
Effect of minCD on FtsZ ring position and polar septation in Bacillus subtilis.
J Bacteriol. 1998 Nov;180(22):6048-51
PMID: 9811667
-
Protein mobility in the cytoplasm of Escherichia coli.
J Bacteriol. 1999 Jan;181(1):197-203
PMID: 9864330
-
Identification and characterization of a negative regulator of FtsZ ring formation in Bacillus subtilis.
Proc Natl Acad Sci U S A. 1999 Aug 17;96(17):9642-7
PMID: 10449747
-
Influence of the nucleoid on placement of FtsZ and MinE rings in Escherichia coli.
J Bacteriol. 2001 Feb;183(4):1413-22
PMID: 11157955
-
The polarity and dynamics of microtubule assembly in the budding yeast Saccharomyces cerevisiae.
Nat Cell Biol. 2000 Jan;2(1):36-41
PMID: 10620805
-
Polymerization of Ftsz, a bacterial homolog of tubulin. is assembly cooperative?
J Biol Chem. 2001 Apr 13;276(15):11743-53
PMID: 11152458
-
Cytological and biochemical characterization of the FtsA cell division protein of Bacillus subtilis.
Mol Microbiol. 2001 Apr;40(1):115-25
PMID: 11298280
-
Bacterial cell division: regulating Z-ring formation.
Mol Microbiol. 2001 May;40(4):795-803
PMID: 11401687
-
Spatial regulation of cytokinesis in bacteria.
Curr Opin Microbiol. 2001 Dec;4(6):647-52
PMID: 11731315
-
Homogeneous expression of the P(BAD) promoter in Escherichia coli by constitutive expression of the low-affinity high-capacity AraE transporter.
Microbiology. 2001 Dec;147(Pt 12):3241-7
PMID: 11739756
-
Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching.
Proc Natl Acad Sci U S A. 2002 Mar 5;99(5):3171-5
PMID: 11854462
-
Asymmetric cell division in B. subtilis involves a spiral-like intermediate of the cytokinetic protein FtsZ.
Cell. 2002 Apr 19;109(2):257-66
PMID: 12007411
-
A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ.
Genes Dev. 2002 Oct 1;16(19):2544-56
PMID: 12368265
-
Cytokinesis in bacteria.
Microbiol Mol Biol Rev. 2003 Mar;67(1):52-65, table of contents
PMID: 12626683
-
Concentration and assembly of the division ring proteins FtsZ, FtsA, and ZipA during the Escherichia coli cell cycle.
J Bacteriol. 2003 Jun;185(11):3344-51
PMID: 12754232
-
In vivo characterization of Escherichia coli ftsZ mutants: effects on Z-ring structure and function.
J Bacteriol. 2003 Aug;185(16):4796-805
PMID: 12896999
-
Essential cell division protein FtsZ assembles into one monomer-thick ribbons under conditions resembling the crowded intracellular environment.
J Biol Chem. 2003 Sep 26;278(39):37664-71
PMID: 12807907
-
Assembly dynamics of the bacterial cell division protein FTSZ: poised at the edge of stability.
Annu Rev Microbiol. 2003;57:125-54
PMID: 14527275
-
Organization of genes in the ftsA-envA region of the Escherichia coli genetic map and identification of a new fts locus (ftsZ).
J Bacteriol. 1980 May;142(2):615-20
PMID: 6991482
-
Tubulin dynamics in cultured mammalian cells.
J Cell Biol. 1984 Dec;99(6):2175-86
PMID: 6501419
-
Microtubule dynamic instability and GTP hydrolysis.
Annu Rev Biophys Biomol Struct. 1992;21:145-66
PMID: 1525467