PrkC modulates MreB filament density and cellular growth rate by monitoring cell wall precursors

Sun, Yingjie; Garner, Ethan C.

doi:10.1101/2020.08.28.272336

Cited by 11 publications

(24 citation statements)

References 35 publications

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“…A regulatory role of peptidoglycan insertion for autolytic activity is supported by previous studies suggesting that the two redundantly essential cell-wall hydrolases of B. subtilis, LytE and CwlO, are controlled by the three MreB homologs (Carballido-López et al, 2006;Domínguez-Cuevas et al, 2013). Furthermore, the amount of moving MreB filaments and cell-envelope growth are highly correlated across different growth conditions (Sun and Garner, 2020), which is compatible with a rate-limiting role of MreB-based cell-wall insertion. However, a molecular mechanism linking cell-wall insertion and cell-wall expansion has not been identified.…”

Section: Introductionsupporting

confidence: 53%

“…In visionary and influential work, Koch (1983) suggested that 'smart autolysins' are activated based on mechanical stress in the cell wall, which, in turn, is caused by turgor pressure. However, more recent works imply that the MreB-linked cell-wall insertion machinery provides the major regulator of cell elongation in B. subtilis (Daniel and Errington, 2003;Billaudeau et al, 2017;Domínguez-Cuevas et al, 2013;Rojas et al, 2017;Sun and Garner, 2020).…”

Section: Introductionmentioning

confidence: 99%

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Cell-envelope synthesis is required for surface-to-mass coupling, which determines dry-mass density inBacillus subtilis

Kitahara

Wilson

et al. 2021

Preprint

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Cells must increase their volumes in response to biomass growth to maintain intracellular mass density, the ratio of dry mass to cell volume, within physiologically permissive bounds. To increase volume, bacteria enzymatically expand their cell envelopes and insert new envelope material. Recently, we demonstrated that the Gram-negative bacterium Escherichia coli expands cell-surface area rather than volume in proportion to mass. Here, we investigate the regulation of cell-volume growth in the evolutionarily distant Bacillus subtilis. First, we demonstrate that the coupling of surface growth to mass growth is conserved in B. subtilis. Therefore, mass density changes with cell shape at the single-cell level. Interestingly, mass density varies by more than 30% when we systematically change cell width by modulation of cell-wall insertion, without any effect on mass-growth rate. Second, we demonstrate that the coupling of surface- and mass growth is broken if peptidoglycan or membrane synthesis are inhibited. Once transient perturbations are relieved, the surface-to-mass ratio is rapidly restored. In conclusion, we demonstrate that surface-to-mass coupling is a conserved principle for volume regulation in bacteria, and that envelope synthesis provides an important link between surface growth and biomass growth in B. subtilis.

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Section: Introductionsupporting

confidence: 53%

Section: Introductionmentioning

confidence: 99%

Cell-envelope synthesis is required for surface-to-mass coupling, which determines dry-mass density inBacillus subtilis

Kitahara

Wilson

et al. 2021

Preprint

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“…Surprisingly, we found that the B. subtilis septal constriction and overall cell growth rate are strongly coupled, with a linear dependence of septal constriction rate on cell growth rate. The molecular mechanism of coupling between septal constriction and cell growth rate requires further research, but possibilities include control of septal synthesis via overall levels of cell wall precursor 41,42 or levels of cell wall synthesis proteins, or direct regulation of cell wall synthesis protein activity via signalling 43 .…”

Section: Discussionmentioning

confidence: 99%

FtsZ treadmilling is essential for Z-ring condensation and septal constriction initiation inBacillus subtiliscell division

Whitley

Jukes

Tregidgo

et al. 2020

Preprint

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ABSTRACTDespite the central role of division in bacterial physiology, how division proteins work together as a nanoscale machine to divide the cell remains poorly understood. Cell division by cell wall synthesis proteins is guided by the cytoskeleton protein FtsZ, which assembles at mid-cell as a dense Z-ring formed of motile treadmilling filaments1,2. However, although FtsZ treadmilling is essential for cell division, the function of FtsZ treadmilling motility remains unclear2–5. Here, we systematically resolve the function of FtsZ treadmilling across each stage of division in the Gram-positive model organism Bacillus subtilis using a novel combination of nanofabrication, advanced microscopy, and microfluidics to measure the division-protein dynamics in live cells with ultrahigh sensitivity. We find that FtsZ treadmilling has two essential functions: mediating condensation of diffuse FtsZ filaments into a dense Z-ring, and initiating constriction by guiding septal cell wall synthesis. After constriction initiation, FtsZ treadmilling has a dispensable function in accelerating septal constriction rate. Our results show that FtsZ treadmilling is critical for assembling and initiating the bacterial cell division machine.

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“…An interesting possibility of precursor availability driving the elongasome activity is suggested, based on the observed interaction of the MurG-MraY complex with MreB (106). Although there is a lack of further evidence for this observation in E. coli, a recent study in B. subtilis shows that MreB filament formation is regulated by RodZ in response to lipid-II abundance, resulting in growth rates that are proportional to nutrient availability (182).…”

Section: Elongation Synthesis: Scaffold Formation By Rod Complexmentioning

confidence: 99%

“…Depletion of elongasome components is lethal in rapidly growing cells due to loss of rod morphology; however, single-gene-deletion mutants are viable and grow poorly as small spheres in nutrient-limiting conditions (183). Interestingly, conditional lethality of mreBCD, rodZ, rodA, and pbp2 is suppressed by overexpression of FtsZ, an essential cytoskeletal factor initiating cell division, which can also be achieved by an increase in cellular concentration of ppGpp, a stationary-phase signaling molecule (164,(175)(176)(177)(178)(179)(180)(181)(182)(183). It is believed that upon inhibition of the elongasome, overexpressed FtsZ may push the cell cycle toward division, bypassing the need for elongation altogether.…”

Section: Elongation Synthesis: Scaffold Formation By Rod Complexmentioning

confidence: 99%

Peptidoglycan: Structure, Synthesis, and Regulation

2021

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Peptidoglycan is a defining feature of the bacterial cell wall. Initially identified as a target of the revolutionary beta-lactam antibiotics, peptidoglycan has become a subject of much interest for its biology, its potential for the discovery of novel antibiotic targets, and its role in infection. Peptidoglycan is a large polymer that forms a mesh-like scaffold around the bacterial cytoplasmic membrane. Peptidoglycan synthesis is vital at several stages of the bacterial cell cycle: for expansion of the scaffold during cell elongation and for formation of a septum during cell division. It is a complex multifactorial process that includes formation of monomeric precursors in the cytoplasm, their transport to the periplasm, and polymerization to form a functional peptidoglycan sacculus. These processes require spatio-temporal regulation for successful assembly of a robust sacculus to protect the cell from turgor and determine cell shape. A century of research has uncovered the fundamentals of peptidoglycan biology, and recent studies employing advanced technologies have shed new light on the molecular interactions that govern peptidoglycan synthesis. Here, we describe the peptidoglycan structure, synthesis, and regulation in rod-shaped bacteria, particularly Escherichia coli , with a few examples from Salmonella and other diverse organisms. We focus on the pathway of peptidoglycan sacculus elongation, with special emphasis on discoveries of the past decade that have shaped our understanding of peptidoglycan biology.

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PrkC modulates MreB filament density and cellular growth rate by monitoring cell wall precursors

Cited by 11 publications

References 35 publications

Cell-envelope synthesis is required for surface-to-mass coupling, which determines dry-mass density inBacillus subtilis

Cell-envelope synthesis is required for surface-to-mass coupling, which determines dry-mass density inBacillus subtilis

FtsZ treadmilling is essential for Z-ring condensation and septal constriction initiation inBacillus subtiliscell division

Peptidoglycan: Structure, Synthesis, and Regulation

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