Bacterial cytokinesis is commonly initiated by the Z-ring, a cytoskeletal structure that assembles at the site of division. Its primary component is FtsZ, a tubulin superfamily GTPase, which is recruited to the membrane by the actin-related protein FtsA. Both proteins are required for the formation of the Z-ring, but if and how they influence each other’s assembly dynamics is not known. Here, we reconstituted FtsA-dependent recruitment of FtsZ polymers to supported membranes, where both proteins self-organize into complex patterns, such as fast-moving filament bundles and chirally rotating rings. Using fluorescence microscopy and biochemical perturbations, we found that these large-scale rearrangements of FtsZ emerge from its polymerization dynamics and a dual, antagonistic role of FtsA: recruitment of FtsZ filaments to the membrane and negative regulation of FtsZ organization. Our findings provide a model for the initial steps of bacterial cell division and illustrate how dynamic polymers can self-organize into large-scale structures.
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We thank the members of the laboratories of T.J.M., T. Bernhardt and T. Rapoport for discussions and support; J. Werbin (Harvard Medical School, USA) for the plasmid for sortase expression; H. Erickson (Duke University, USA) for the plasmid for FtsZ–YFP–mts expression; J. Brugues for valuable discussions and advice; and E. Garner, K. Kruse and S. Grill for discussions and comments on the manuscript. We would also like to thank the Nikon Imaging Center at Harvard Medical School for their excellent service. M.L. is supported by fellowships from EMBO (ALTF 394-2011) and HFSP (LT000466/2012). Cytoskeleton dynamics research in the T.J.M. group is supported by NIH-GM39565.
The authors declare no competing financial interests.
Integrated supplementary information
(a) Illustration of protein interactions lipids (adapted from ref. 20): FtsA and ZipA bind to same highly conserved C-tail of FtsZ (shown in green), which is connected to the rest of the protein by a flexible linker.FtsA binds to the membrane surface using an amphipathix helix, located at the end of a C-terminal flexible linker. ZipA is a transmembrane protein. The N-terminal transmembrane-domain has been substituted by a His-tag obtaining His-Δ22-ZipA, which was then permanently attached to the membrane using Ni2+ chelating. (b) Commassie-stained SDS-Page gel of purified proteins used for this study. (c) Schematic drawing of the experimental assay. A plastic ring was glued to a glass cover slip to create a reaction chamber and a supported lipid bilayer was formed on the glass surface. FtsA, FtsZ and ATP were added to the buffer before polymerization of FtsZ was initiated by adding GTP.
Supplementary Figure 2 Remodeling of cytoskeletal structures depends on the presence of ATP, but not on FtsA polymerization.
(a) Representative intensity curve corresponding to Supplementary Video 4, showing the role of ATP for FtsZ–FtsA co-assembly: The initial transient binding of FtsZ to the membrane is likely due to residual amounts of ATP being co-purified with FtsA. After detachment of FtsZ and FtsA, the filament network reassembled as soon as fresh ATP is added (at orange arrowhead and dashed line). Similar intensity curves were obtained in 5 experiments. (b) FtsA polymerization is not important for the self-organization of FtsZ and FtsA in our in vitro system. When we used self-interaction mutants of FtsA (FtsA R286W (left), FtsA M167I (middle), FtsA V277M (right)), FtsZ formed the same cytoskeletal pattern as with the wildtype protein. Similar micrographs were obtained in n = 10 experiments.
Snapshots, maximum intensity projections (MIP) and kymographs of single FtsZ filaments from movies acquired at a frame-rate of 2s or 400 ms (FtsZ = 0.45 μM with 30 mol-% FtsZ-Alexa488, FtsA = 0.2 μM). Cyan arrowheads in MIPs indicate the first binding of FtsZ to the membrane. Yellow arrows in kymograph show the polymerization direction. Top left, with grey background. Scale bars correspond to 500 nm or 5 s. Values in grey box (top left) represent average values of n = 38 analyzed filaments from 5 independent experiments.
Supplementary Figure 4 Influence of different concentrations of membrane anchors on FtsZ filament patterns.
(a) Representative snapshots of FtsZ filaments recruited to the membrane by ZipA at indicated time points after addition of GTP. The percentage of Ni2+-chelating lipids (18:1 DGS-NTA-Ni2+) defines the amount of ZipA immobilized and the amount of FtsZ recruited to the membrane. With 8% Ni2+ chelating lipids, FtsZ bundles densely covered the membrane. At lower concentrations (1%, 2% and 4%), bundles of FtsZ filaments start to appear after about 20 min. On membranes with 1% Ni2+-chelating lipids, individual FtsZ filaments could briefly be resolved (see 3 min after addition of GTP), before the filament density became too high. Similar micrographs were obtained in 5 experiments. (b) Simplified phase diagram of FtsZ–FtsA filament networks on the membrane. Filled green dots represent experiments with protein concentrations allowing for the formation of a dynamic filament network (at protein concentrations of [FtsZ]>0.7 μM and 0.125 μM<[FtsA]<1.7 μM). Empty dots represent experiments where FtsZ filaments were either too short for a continuous polymer network (with FtsZ<0.7 μM) or where they did not show rapid rearrangements (with FtsA<0.125 μM). Light green area represents the concentration ratio for FtsA and FtsZ found in vivo26. Yellow filled circle represents the concentration ratio used for single FtsZ filament experiments. (c) Representative snapshots and overlays of two individual frames separated by 2 min of a time-lapse movie. At low FtsA concentrations (top), FtsZ forms static, long filaments, whereas at high FtsA concentrations (bottom), filaments were short and dynamic, but did not form a continuous filament network. Similar micrographs were obtained in 5 experiments.
Supplementary Figure 5 The membrane anchor does not influence the GTPase rate and lifetime of FtsZ monomers.
(a) With ZipA, the average lifetime of FtsZ was slightly longer than with FtsA. Linear-log plot of FtsZ lifetime distribution with ZipA as membrane anchor (filled red circles) about 30 min after addition of GTP. Black line represents the averaged linear fit to individual lifetime distributions with <t> = 10.68 s±2.33 s (s.d. n = 24 videos with 1500 particles obtained from 5 independent experiments), which is slightly longer than for FtsZ/FtsA (p = 0.0174). (b) FtsZ GTPase activity was not affected by the membrane anchor. Bar graph shows GTPase activity of FtsZ (5 μM) or FtsZ-YFP-MTS (5 μM) and the influence of membrane anchors (His-ZipA or FtsA, 3 μM) and phospholipids (1 mg ml−1). The corresponding rates were normalized to the GTP activity of FtsZ alone (0.083/s). We found that the GTPase activity of FtsZ-YFP-MTS to be about 30% lower than of wildtype FtsZ. GTPase activities were determined using the EnzChek Phosphate Assay Kit (Molecular Probes). Error bars correspond to s.d, from n = 3 independent experiments.
Left, mean intensity traces for FtsZ depolymerization upon rapid dilution for FtsZ filaments recruited to the membrane by ZipA and FtsA. Right: mean disassembly times obtained from double-exponential fits, error bars and thin lines correspond to s.e.m, (n = 3 independent experiments). Bottom: Representative snapshots showing disassembly of FtsZ filaments after dilution (time point of dilution is indicated by orange arrowhead and dashed line). In the presence of both anchors, ZipA and FtsA, no thick bundles of FtsZ persist on the membrane. Fluorescence intensity of each frame was normalized.
Supplementary Figure 7 Uncropped Commassie-stained SDS-Page gels corresponding to Fig. 3c (a) and 4d (b).
P = Pellet, SN = Supernatant; 1 and 1’ in bindicate replicates using identical experimental conditions.
Supplementary Information (PDF 1754 kb)
Supplementary Information (XLSX 55 kb)
Supplementary Information (XLSX 29 kb)
Video of FtsZ–FtsA filament pattern formation after addition of GTP (FtsZ = 1.5 μM with 30 mol-% FtsZ-Alexa488, FtsA = 0.5 μM. Note that Video was normalized to have a constant overall intensity, thus compensating for the increasing intensity over time due to protein binding to the membrane. As a consequence of this normalization, non-specific bound fluorescent particles appear disproportionately bright at the beginning of a Video. Scale bar is 10 μm. (MOV 29548 kb)
Close up of Supplementary Video 1. Scale bar is 1 μm. (MOV 2743 kb)
Video corresponds to Fig. 1c (FtsZ = 1.5 μM with 30 mol-% FtsZ-Alexa488, FtsA = 0.5 μM). Scale bar is 10 μm. (MOV 15932 kb)
Video corresponds to Supplementary Fig. 2a. Scale bar is 5 μm. (MOV 6782 kb)
The FtsZ–FtsA filament network does not show rapid rearrangements in the presence of GMPCPP, a non-hydrolyzable analog of GTP (FtsZ = 1.5 μM with 30 mol-% FtsZ-Alexa488, FtsA = 0.5 μM). Scale bar is 5 μm. (MOV 1265 kb)
While the protein network is reorganizing, individual FtsZ proteins remain at the same position (FtsZ, 1.25 μM with 30 mol-% FtsZ-Alexa488 and 0.4 mol-% FtsZ-Cy5; FtsA, 0.4 μM). Scale bar is 10 μm. (MOV 9610 kb)
Close up of Supplementary Video 6 showing single FtsZ monomers in a rotating ring of FtsZ filaments.
Scale bar is 3 μm. (MOV 6289 kb)
Dynamics of individual Cy5-labeled FtsZ proteins in a dynamic network at higher frame-rate (360 ms/frame) (FtsZ, 1.25 μM with 0.4 mol-% FtsZ-Cy5; FtsA, 0.4 μM). Scale bar is 5 μm. (MOV 11369 kb)
(FtsZ = 0.45 μM with 30 mol-% FtsZ-Alexa488, FtsA = 0.2 μM). Scale bar is 5 μm. (MOV 16952 kb)
A polymer network formed with autonomously binding FtsZ does not show large-scale reorganizations (mts = membrane targeting sequence, FtsZ-YFP-mts = 1.25 μM). Scale bar is 5 μm. (MOV 3911 kb)
In contrast to FtsA, ZipA does not allow for rapid rearrangement of the cytoskeletal pattern. Instead FtsZ forms a static network of dynamic FtsZ filaments (FtsZ = 1.5 μM with 30 mol-% FtsZ-Alexa488; His-Δ22-ZipA 0.5 μM, supported membrane contained 4 mol-% Ni-chelating lipids). Scale bar is 5 μm. (MOV 30516 kb)
Video corresponds to Fig. 4a (FtsZ = 1.5 μM with 30 mol-% FtsZ-Alexa488, FtsA = 0.5 μM with 10 % Cy5-GG-FtsA). Left: merged channels; center: FtsZ-Alexa488, right: Cy5-GG-FtsA. Scale bar is 5 μm. (MOV 12577 kb)
FtsZ = 0.45 μM with 30 mol-% FtsZ-Alexa488, FtsA = 0.2 μM with 10% Cy5-GG-FtsA. Left: merged channels; center: FtsZ-Alexa488, right: Cy5-GG-FtsA. Scale bar is 5 μm. (MOV 8772 kb)
Video corresponds to graph in Fig. 4c (FtsZ = 1 μM with 30 mol-% FtsZ-Alexa488, FtsA = 0.3 μM with 10 % Cy5-GG-FtsA) (final concentrations). FtsZ was added at 19 min (at change in xy-position). Left: merged channels; center: FtsZ-Alexa488, right: Cy5-GG-FtsA. Scale bar is 5 μm. (MOV 37672 kb)
Video of FtsZ filament network formation with FtsA-Δ15-6xHis as membrane anchor (FtsZ = 1.5 μM with 30 mol-% FtsZ-Alexa488; FtsA-Δ15-6xHis 0.5 rmmuM, supported membrane contained 4 mol-% Ni-chelating lipids). Scale bar is 5 μm. (MOV 14898 kb)
Top: Video corresponding to graph in Fig. 5a showing the disassembly of preformed FtsZ filaments after addition of FtsA (FtsZ = 1.2 μM with 30 mol-% FtsZ-Alexa488, FtsA = 0.3 μM with 10 % Cy5-GG-FtsA, final concentrations). Left: merged channels; center: FtsZ-Alexa488, right: Cy5-GG-FtsA. Bottom: Video corresponding to graph in Fig. 5b showing the assembly of an FtsZ filament network after addition of ZipA. (FtsZ = 1.2 μMwith 30 mol-% FtsZ-Alexa488, His-Δ22-ZipA = 0.3 μM, final concentrations, supported membrane contained 4 mol-% Ni-chelating lipids). Scale bar is 5 μm. (MOV 26951 kb)
Videos of rapid dilution experiment showing disassembly of FtsZ filaments after 5-fold volume increase of the buffer. For the Videos in the top row, the intensities of each frame were normalized to visualize the architecture of FtsZ filaments after dilution. The bottom row shows the raw data. Left column: Disassembly of FtsZ-ZipA. Sample was diluted between 5 and 10 sec. Right column: Disassembly of FtsZ–FtsA. Sample was diluted between 45 and 50 sec. Scale bar is 2 μm. (MOV 2931 kb)
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Loose, M., Mitchison, T. The bacterial cell division proteins FtsA and FtsZ self-organize into dynamic cytoskeletal patterns. Nat Cell Biol 16, 38–46 (2014). https://doi.org/10.1038/ncb2885
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