Supramolecular structure in the membrane of Staphylococcus aureus

Abstract

All life demands the temporal and spatial control of essential biological functions. In bacteria, the recent discovery of coordinating elements provides a framework to begin to explain cell growth and division. Here we present the discovery of a supramolecular structure in the membrane of the coccal bacterium Staphylococcus aureus, which leads to the formation of a largescale pattern across the entire cell body; this has been unveiled by studying the distribution of essential proteins involved in lipid metabolism (PlsY and CdsA). The organization is found to require MreD, which determines morphology in rod-shaped cells. The distribution of protein complexes can be explained as a spontaneous pattern formation arising from the competition between the energy cost of bending that they impose on the membrane, their entropy of mixing, and the geometric constraints in the system. Our results provide evidence for the existence of a self-organized and nonpercolating molecular scaffold involving MreD as an organizer for optimal cell function and growth based on the intrinsic self-assembling properties of biological molecules.T he perpetuation of all cellular life requires the temporal and spatial management of essential biological functions, within the morphological framework characteristic of a specific organism. The underlying processes, which determine cell shape, are intimately intertwined with cell division and constitute pivotal issues for cell biology; their coordination in prokaryotes is mediated through counterparts of eukaryotic actin, tubulin, and intermediate filaments in addition to other specific components (1, 2). Several of these apparent cytoskeletal elements capitalize on their membrane binding properties, assembling along the longitudinal axis, between the poles of rod-shaped cells; they participate in many processes, including selection of the division site via the Min system and other components (3, 4); guidance and control of the cell wall biosynthetic machinery responsible for cell size, polarity, and shape through the actin-like protein MreB (5-11); and chromosome partitioning into daughter cells using another actin-like filament, ParM (12).Despite this set of highly coordinated mechanisms, it has recently been shown that otherwise rod-and cocci-shaped bacteria can exist as largely spherical wall-less forms known as L-forms, with the capacity to divide (13). Importantly, the division of L-forms of the rod-shaped bacterium Bacillus subtilis is freed from the requirement of the classical tubulin-like division component FtsZ (14). L-forms appear to divide by scission after blebbing, tabulation, or vesiculation dependent on an altered rate of membrane biosynthesis (15); this harks back perhaps to a more evolutionary primitive mechanism permitting cellular proliferation. Thus, are there underlying organizational mechanisms that exist, independent of apparent cytoskeletal elements? The fluid mosaic model proposing the free diffusion of membrane proteins through the lipids has been challenged by growing e...

Pattern formation by curvature-inducing proteins on spherical membranes

“…Such patterns have been observed in L-form [6,7] bacteria, as well as in coccal bacteria [5]. The patterns formed by PlsY and CdsA proteins (both essential to lipid metabolism) in Staphylococcus aureus, in particular, show a striking coupling between protein density and membrane curvature [12]. As seen in figures 4 and 5, and determined from (34), modes with  ℓ 10 are expected for >´-P 1.4 10 4 which, for a typical cell size of m = R 1 m, would correspond to correlation lengths x > 10 nm, well within the biologically plausible range.…”

“…Very recently, [12] a system was identified in which cell polarisation appears to be controlled by a relatively simple pattern-formation mechanism. In the coccal bacterium Staphylococcus aureus, essential proteins involved in lipid metabolism were seen to distribute in inhomogeneous spatial patterns, that could be explained by a model that considers the dynamics of curvature-inducing proteins on a spherical membrane.…”

“…In the coccal bacterium Staphylococcus aureus, essential proteins involved in lipid metabolism were seen to distribute in inhomogeneous spatial patterns, that could be explained by a model that considers the dynamics of curvature-inducing proteins on a spherical membrane. However, the model first introduced in [12] is very general, and we expect that it might be able to describe the formation of 2. Methods…”

Nigella sativa essential oil and its bioactive compounds as resistance modifiers against Staphylococcus aureus

“…The distribution of essential proteins involved in lipid metabolism (PlsY and CdsA) may be different in ATCC and MRSA isolates; this is the reason for the different properties of EO and Thq regarding membrane damaging effect (García‐Lara et al, ). It has been reported previously that the antibacterial potential of the natural compound caffeic acid is different based on the resistant and reference ATCC strain of the same species, namely, S. aureus (Kępa et al, ).…”

Identification of pneumococcal proteins that are functionally linked to penicillin‐binding protein 2b (PBP2b)

“…In a recent paper, García‐Lara et al . () reports that a Staphylococcus aureus Δ mreC mutant grows identically to the parental strain, while lack of MreD leads to growth defects and abnormal cell morphology. This is very similar to the phenotypes we observe for the pneumococcal mreC and mreD mutants.…”