MreB-Dependent Organization of the E. coli Cytoplasmic Membrane Controls Membrane Protein Diffusion

Oswald, Felix; Varadarajan, Aravindan; Lill, Holger; Peterman, Erwin J. G.; Bollen, Yves J.M.

doi:10.1016/j.bpj.2016.01.010

Cited by 77 publications

(101 citation statements)

References 55 publications

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“…7). As a result, the diffusive behavior of FloA and FloT assemblies resembles the classical pattern observed in eukaryotic membranes: random diffusion of proteins over short timescales 97 with reduced diffusivity or subdiffusion over longer timescales 52,98–100 . Notably, FloT diffusivity is lower than FloA on longer timescales.…”

Section: Discussionmentioning

confidence: 61%

“…Our work provides evidence that prokaryotes and eukaryotes share fundamental mechanisms of membrane compartmentalization, presumably to maintain efficient protein-protein interactions, assist in the oligomerization of protein complexes for the optimal organization of cellular processes and metabolism, and to help avoid unfavorable protein stoichiometries and unwanted protein interactions. The cortical and cell-wall cytoskeletal structures act as effective barriers against the diffusion of membrane microdomains in both eukaryotes and prokaryotes 51,52 .…”

Section: Discussionmentioning

confidence: 99%

“…How bacterial cells ensure that their FMMs are correctly distributed in the cellular membrane is poorly understood. Actin-like MreB and its homologs MreBH and Mbl are key components of the bacterial cytoskeleton and play an important role in bacterial membrane organization 51,52 . They form filaments underneath the membrane and interact with integral membrane proteins, such as the mreB operon partners MreCD and cell wall synthesis proteins such as RodZ, the penicillin-binding proteins (PBPs) PBPH, PBP2a and SEDS (shape, elongation, division and sporulation) proteins 53–57 .…”

Section: Introductionmentioning

confidence: 99%

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The Bacterial Cytoskeleton Spatially Confines Functional Membrane Microdomains

Machta

et al. 2020

Preprint

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22Cell membranes laterally segregate into microdomains enriched in certain lipids and scaffold 23 proteins. Membrane microdomains modulate protein-protein interactions and are essential for cell 24 polarity, signaling and membrane trafficking. How cells organize their membrane microdomains, and 25 the physiological importance of these microdomains, is unknown. In eukaryotes, the cortical actin 26 cytoskeleton is proposed to act like a fence, constraining the dynamics of membrane microdomains. 27Like their eukaryotic counterparts, bacterial cells have functional membrane microdomains (FMMs) 28 that act as platforms for the efficient oligomerization of protein complexes. In this work, we used the 29 model organism Bacillus subtilis to demonstrate that FMM organization and movement depend 30 primarily on the interaction of FMM scaffold proteins with the domains' protein cargo, rather than with 31 domain lipids. Additionally, the MreB actin-like cytoskeletal network that underlies the bacterial 32 membrane was found to frame areas of the membrane in which FMM mobility is concentrated. 33Variations in membrane fluidity did not affect FMM mobility whereas alterations in cell wall organization 34 affected FMM mobility substantially. Interference with MreB organization alleviates FMM spatial 35 confinement whereas, by contrast, inhibition of cell wall synthesis strengthens FMM confinement. The 36 restriction of FMM lateral mobility by the submembranous actin-like cytoskeleton or the extracellular 37 wall cytoskeleton appears to be a conserved mechanism in prokaryotic and eukaryotic cells for 38 localizing functional protein complexes in specific membrane regions, thus contributing to the 39 organization of cellular processes. 40 41 42 43 48 actually heterogeneous fluids, with different membrane lipid species laterally segregating into sub-49 micrometer domains, driven by their physico-chemical properties 2-4 . This heterogeneous organization 50 of membrane lipids leads to a heterogeneous distribution of the embedded membrane proteins, which 51 appears essential for their functionality 5 . Membrane microdomains are widely present, mobile 52 structures that vary in size from transient protein clusters measured in nm 6 to large micron-sized stable 53 domains such as desmosomes 7 . These domains harbor proteins specialized in membrane trafficking, 54 cell-cell adhesion, and signal transduction, and they provide targets for viral entry 8 . 56It is now appreciated that membrane proteins can significantly impact membrane organization, in 57 particular stabilizing membrane domains. For instance, the scaffold activity of the flotillin proteins FLO1 58 and FLO2 plays an important role in stabilizing some eukaryotic membrane rafts ("lipid rafts") 9-11 ; it 59 would seem that this raft organization occurs in part through the capture and stabilization of specific 60 lipids by flotillins 12,13 . In addition, the activity of the flotillin scaffold contributes to the recruitment of 61 other raft-associated proteins, thus facilitatin...

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Section: Discussionmentioning

confidence: 61%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The Bacterial Cytoskeleton Spatially Confines Functional Membrane Microdomains

Machta

et al. 2020

Preprint

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“…GlpT (glycerol‐3‐phosphate transporter) is the major transporter for the uptake of sn ‐glycerol 3‐phosphate in E. coli . It was reported to have 12 TMHs and to function as monomer (Huang, ), which diffuses homogenously in the IM (Oswald et al, ). It was therefore expected to show homogenous membrane localization.…”

Section: Resultsmentioning

confidence: 99%

FtsW activity and lipid II synthesis are required for recruitment of MurJ to midcell during cell division in Escherichia coli

Liu

Meiresonne

Bouhss

et al. 2018

Molecular Microbiology

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Peptidoglycan (PG) is the unique cell shape-determining component of the bacterial envelope, and is a key target for antibiotics. PG synthesis requires the transmembrane movement of the precursor lipid II, and MurJ has been shown to provide this activity in Escherichia coli. However, how MurJ functions in vivo has not been reported. Here we show that MurJ localizes both in the lateral membrane and at midcell, and is recruited to midcell simultaneously with late-localizing divisome proteins and proteins MraY and MurG. MurJ septal localization is dependent on the presence of a complete and active divisome, lipid II synthesis and PBP3/FtsW activities. Inactivation of MurJ, either directly by mutation or through binding with MTSES, did not affect the midcell localization of MurJ. Our study visualizes MurJ localization in vivo and reveals a possible mechanism of MurJ recruitment during cell division.

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“…24), indicating that other interactions act to reduce the effective diffusion constants; a recent study observed that diffusion of a set of membrane proteins in E. coli cells was MreB-dependent and in the range 0.026–0.21 μm 2 s −1 (ref. 25). The PBP1A MSD saturated after 0.2–0.3 s (Fig.…”

Section: Resultsmentioning

confidence: 99%

Single-molecule imaging reveals modulation of cell wall synthesis dynamics in live bacterial cells

et al. 2016

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The peptidoglycan cell wall is an integral organelle critical for bacterial cell shape and stability. Proper cell wall construction requires the interaction of synthesis enzymes and the cytoskeleton, but it is unclear how the activities of individual proteins are coordinated to preserve the morphology and integrity of the cell wall during growth. To elucidate this coordination, we used single-molecule imaging to follow the behaviours of the two major peptidoglycan synthases in live, elongating Escherichia coli cells and after perturbation. We observed heterogeneous localization dynamics of penicillin-binding protein (PBP) 1A, the synthase predominantly associated with cell wall elongation, with individual PBP1A molecules distributed between mobile and immobile populations. Perturbations to PBP1A activity, either directly through antibiotics or indirectly through PBP1A's interaction with its lipoprotein activator or other synthases, shifted the fraction of mobile molecules. Our results suggest that multiple levels of regulation control the activity of enzymes to coordinate peptidoglycan synthesis.

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MreB-Dependent Organization of the E. coli Cytoplasmic Membrane Controls Membrane Protein Diffusion

Cited by 77 publications

References 55 publications

The Bacterial Cytoskeleton Spatially Confines Functional Membrane Microdomains

The Bacterial Cytoskeleton Spatially Confines Functional Membrane Microdomains

FtsW activity and lipid II synthesis are required for recruitment of MurJ to midcell during cell division in Escherichia coli

Single-molecule imaging reveals modulation of cell wall synthesis dynamics in live bacterial cells

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