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Bistable forespore engulfment in Bacillus subtilis by a zipper mechanism in absence of the cell wall.

Ojkic N, López-Garrido J, Pogliano K, Endres RG - PLoS Comput. Biol. (2014)

Bottom Line: By systematic exploration of model parameters, we predict regions of osmotic pressure and membrane-surface tension that produce successful engulfment.Indeed, decreasing the medium osmolarity in experiments prevents engulfment in line with our predictions.Forespore engulfment may thus not only be an ideal model system to study decision-making in single cells, but its biophysical principles are likely applicable to engulfment in other cell types, e.g. during phagocytosis in eukaryotes.

View Article: PubMed Central - PubMed

Affiliation: Department of Life Sciences, Imperial College, London, United Kingdom; Centre for Integrative Systems Biology and Bioinformatics, Imperial College, London, United Kingdom.

ABSTRACT
To survive starvation, the bacterium Bacillus subtilis forms durable spores. The initial step of sporulation is asymmetric cell division, leading to a large mother-cell and a small forespore compartment. After division is completed and the dividing septum is thinned, the mother cell engulfs the forespore in a slow process based on cell-wall degradation and synthesis. However, recently a new cell-wall independent mechanism was shown to significantly contribute, which can even lead to fast engulfment in [Formula: see text] 60 [Formula: see text] of the cases when the cell wall is completely removed. In this backup mechanism, strong ligand-receptor binding between mother-cell protein SpoIIIAH and forespore-protein SpoIIQ leads to zipper-like engulfment, but quantitative understanding is missing. In our work, we combined fluorescence image analysis and stochastic Langevin simulations of the fluctuating membrane to investigate the origin of fast bistable engulfment in absence of the cell wall. Our cell morphologies compare favorably with experimental time-lapse microscopy, with engulfment sensitive to the number of SpoIIQ-SpoIIIAH bonds in a threshold-like manner. By systematic exploration of model parameters, we predict regions of osmotic pressure and membrane-surface tension that produce successful engulfment. Indeed, decreasing the medium osmolarity in experiments prevents engulfment in line with our predictions. Forespore engulfment may thus not only be an ideal model system to study decision-making in single cells, but its biophysical principles are likely applicable to engulfment in other cell types, e.g. during phagocytosis in eukaryotes.

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Engulfment model and Langevin simulations.(A) 3D mother-cell membrane is represented by a string of beads assuming rotational symmetry around -axis. Each bead at position (, ) represents a ribbon of width  and length . Forespore is modeled as a solid sphere. See Materials and Methods, and Text S1 for further model explanations. (B) Snapshot of 3D simulation showing example of early-stage engulfment.
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pcbi-1003912-g004: Engulfment model and Langevin simulations.(A) 3D mother-cell membrane is represented by a string of beads assuming rotational symmetry around -axis. Each bead at position (, ) represents a ribbon of width and length . Forespore is modeled as a solid sphere. See Materials and Methods, and Text S1 for further model explanations. (B) Snapshot of 3D simulation showing example of early-stage engulfment.

Mentions: In our model the 3D mother-cell membrane is represented by a string of beads assuming rotational symmetry around the -axis, while the forespore membrane was modeled as a hard sphere (Fig. 4). Indeed, experiments show negligible deformation of the forespore during engulfment (Fig. 2A and B). Specifically, the Langevin dynamic equation of the bead at position is given by:


Bistable forespore engulfment in Bacillus subtilis by a zipper mechanism in absence of the cell wall.

Ojkic N, López-Garrido J, Pogliano K, Endres RG - PLoS Comput. Biol. (2014)

Engulfment model and Langevin simulations.(A) 3D mother-cell membrane is represented by a string of beads assuming rotational symmetry around -axis. Each bead at position (, ) represents a ribbon of width  and length . Forespore is modeled as a solid sphere. See Materials and Methods, and Text S1 for further model explanations. (B) Snapshot of 3D simulation showing example of early-stage engulfment.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4214620&req=5

pcbi-1003912-g004: Engulfment model and Langevin simulations.(A) 3D mother-cell membrane is represented by a string of beads assuming rotational symmetry around -axis. Each bead at position (, ) represents a ribbon of width and length . Forespore is modeled as a solid sphere. See Materials and Methods, and Text S1 for further model explanations. (B) Snapshot of 3D simulation showing example of early-stage engulfment.
Mentions: In our model the 3D mother-cell membrane is represented by a string of beads assuming rotational symmetry around the -axis, while the forespore membrane was modeled as a hard sphere (Fig. 4). Indeed, experiments show negligible deformation of the forespore during engulfment (Fig. 2A and B). Specifically, the Langevin dynamic equation of the bead at position is given by:

Bottom Line: By systematic exploration of model parameters, we predict regions of osmotic pressure and membrane-surface tension that produce successful engulfment.Indeed, decreasing the medium osmolarity in experiments prevents engulfment in line with our predictions.Forespore engulfment may thus not only be an ideal model system to study decision-making in single cells, but its biophysical principles are likely applicable to engulfment in other cell types, e.g. during phagocytosis in eukaryotes.

View Article: PubMed Central - PubMed

Affiliation: Department of Life Sciences, Imperial College, London, United Kingdom; Centre for Integrative Systems Biology and Bioinformatics, Imperial College, London, United Kingdom.

ABSTRACT
To survive starvation, the bacterium Bacillus subtilis forms durable spores. The initial step of sporulation is asymmetric cell division, leading to a large mother-cell and a small forespore compartment. After division is completed and the dividing septum is thinned, the mother cell engulfs the forespore in a slow process based on cell-wall degradation and synthesis. However, recently a new cell-wall independent mechanism was shown to significantly contribute, which can even lead to fast engulfment in [Formula: see text] 60 [Formula: see text] of the cases when the cell wall is completely removed. In this backup mechanism, strong ligand-receptor binding between mother-cell protein SpoIIIAH and forespore-protein SpoIIQ leads to zipper-like engulfment, but quantitative understanding is missing. In our work, we combined fluorescence image analysis and stochastic Langevin simulations of the fluctuating membrane to investigate the origin of fast bistable engulfment in absence of the cell wall. Our cell morphologies compare favorably with experimental time-lapse microscopy, with engulfment sensitive to the number of SpoIIQ-SpoIIIAH bonds in a threshold-like manner. By systematic exploration of model parameters, we predict regions of osmotic pressure and membrane-surface tension that produce successful engulfment. Indeed, decreasing the medium osmolarity in experiments prevents engulfment in line with our predictions. Forespore engulfment may thus not only be an ideal model system to study decision-making in single cells, but its biophysical principles are likely applicable to engulfment in other cell types, e.g. during phagocytosis in eukaryotes.

Show MeSH
Related in: MedlinePlus