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From cell differentiation to cell collectives: Bacillus subtilis uses division of labor to migrate.

van Gestel J, Vlamakis H, Kolter R - PLoS Biol. (2015)

Bottom Line: We propose that surfactin-producing cells reduce the friction between cells and their substrate, thereby facilitating matrix-producing cells to form bundles.Our study illustrates how the simple organization of cells within a community can yield a strong ecological advantage.This is a key factor underlying the diverse origins of multicellularity.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology and Immunobiology, Harvard Medical School, Boston, Massachusetts, United States of America; Theoretical Biology Group, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands.

ABSTRACT
The organization of cells, emerging from cell-cell interactions, can give rise to collective properties. These properties are adaptive when together cells can face environmental challenges that they separately cannot. One particular challenge that is important for microorganisms is migration. In this study, we show how flagellum-independent migration is driven by the division of labor of two cell types that appear during Bacillus subtilis sliding motility. Cell collectives organize themselves into bundles (called "van Gogh bundles") of tightly aligned cell chains that form filamentous loops at the colony edge. We show, by time-course microscopy, that these loops migrate by pushing themselves away from the colony. The formation of van Gogh bundles depends critically on the synergistic interaction of surfactin-producing and matrix-producing cells. We propose that surfactin-producing cells reduce the friction between cells and their substrate, thereby facilitating matrix-producing cells to form bundles. The folding properties of these bundles determine the rate of colony expansion. Our study illustrates how the simple organization of cells within a community can yield a strong ecological advantage. This is a key factor underlying the diverse origins of multicellularity.

No MeSH data available.


Related in: MedlinePlus

Model of filament growth and migration.Upper left: microscopy image of WT cells on the edge of the colony taken 18 h after inoculation. Lower left: relative migration rate for three parameter settings: (A) default parameter setting (grey), (B) high bending rigidity between cells (blue), and (C) large cell size (dark blue). Histograms and error bars show, respectively, mean and standard deviation (n = 10) in the extent of migration along the y-axis of the two-dimensional space (see images on the right; filament growth is initiated on the bottom). Right: filamentous loops at the end of the simulation for three representative runs, one for each of the three different parameter settings. See Materials and Methods for detailed model description and exact parameter settings (S2 Table).
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pbio.1002141.g010: Model of filament growth and migration.Upper left: microscopy image of WT cells on the edge of the colony taken 18 h after inoculation. Lower left: relative migration rate for three parameter settings: (A) default parameter setting (grey), (B) high bending rigidity between cells (blue), and (C) large cell size (dark blue). Histograms and error bars show, respectively, mean and standard deviation (n = 10) in the extent of migration along the y-axis of the two-dimensional space (see images on the right; filament growth is initiated on the bottom). Right: filamentous loops at the end of the simulation for three representative runs, one for each of the three different parameter settings. See Materials and Methods for detailed model description and exact parameter settings (S2 Table).

Mentions: As shown in Fig 10, these three simple cell-level behaviors are sufficient to produce expanding filamentous loops at the colony edge that look surprisingly similar to those observed in our experiments. Cell elongation and division result in undulations of the filaments (i.e., regions where the filaments bend slightly inwards or outwards). These undulations get smoothened as long as neighboring cells resist bending by strongly aligning with respect to each other (i.e., bending rigidity). However, when growth continues, the filament gets compressed and undulations increase. As a consequence, the filament starts folding. The folds turn into loops, which expand in space. As observed in the experimental results (Figs 8–10), the model gives rise to bigger loops at the edge of the colony (Fig 10).


From cell differentiation to cell collectives: Bacillus subtilis uses division of labor to migrate.

van Gestel J, Vlamakis H, Kolter R - PLoS Biol. (2015)

Model of filament growth and migration.Upper left: microscopy image of WT cells on the edge of the colony taken 18 h after inoculation. Lower left: relative migration rate for three parameter settings: (A) default parameter setting (grey), (B) high bending rigidity between cells (blue), and (C) large cell size (dark blue). Histograms and error bars show, respectively, mean and standard deviation (n = 10) in the extent of migration along the y-axis of the two-dimensional space (see images on the right; filament growth is initiated on the bottom). Right: filamentous loops at the end of the simulation for three representative runs, one for each of the three different parameter settings. See Materials and Methods for detailed model description and exact parameter settings (S2 Table).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4403855&req=5

pbio.1002141.g010: Model of filament growth and migration.Upper left: microscopy image of WT cells on the edge of the colony taken 18 h after inoculation. Lower left: relative migration rate for three parameter settings: (A) default parameter setting (grey), (B) high bending rigidity between cells (blue), and (C) large cell size (dark blue). Histograms and error bars show, respectively, mean and standard deviation (n = 10) in the extent of migration along the y-axis of the two-dimensional space (see images on the right; filament growth is initiated on the bottom). Right: filamentous loops at the end of the simulation for three representative runs, one for each of the three different parameter settings. See Materials and Methods for detailed model description and exact parameter settings (S2 Table).
Mentions: As shown in Fig 10, these three simple cell-level behaviors are sufficient to produce expanding filamentous loops at the colony edge that look surprisingly similar to those observed in our experiments. Cell elongation and division result in undulations of the filaments (i.e., regions where the filaments bend slightly inwards or outwards). These undulations get smoothened as long as neighboring cells resist bending by strongly aligning with respect to each other (i.e., bending rigidity). However, when growth continues, the filament gets compressed and undulations increase. As a consequence, the filament starts folding. The folds turn into loops, which expand in space. As observed in the experimental results (Figs 8–10), the model gives rise to bigger loops at the edge of the colony (Fig 10).

Bottom Line: We propose that surfactin-producing cells reduce the friction between cells and their substrate, thereby facilitating matrix-producing cells to form bundles.Our study illustrates how the simple organization of cells within a community can yield a strong ecological advantage.This is a key factor underlying the diverse origins of multicellularity.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology and Immunobiology, Harvard Medical School, Boston, Massachusetts, United States of America; Theoretical Biology Group, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands.

ABSTRACT
The organization of cells, emerging from cell-cell interactions, can give rise to collective properties. These properties are adaptive when together cells can face environmental challenges that they separately cannot. One particular challenge that is important for microorganisms is migration. In this study, we show how flagellum-independent migration is driven by the division of labor of two cell types that appear during Bacillus subtilis sliding motility. Cell collectives organize themselves into bundles (called "van Gogh bundles") of tightly aligned cell chains that form filamentous loops at the colony edge. We show, by time-course microscopy, that these loops migrate by pushing themselves away from the colony. The formation of van Gogh bundles depends critically on the synergistic interaction of surfactin-producing and matrix-producing cells. We propose that surfactin-producing cells reduce the friction between cells and their substrate, thereby facilitating matrix-producing cells to form bundles. The folding properties of these bundles determine the rate of colony expansion. Our study illustrates how the simple organization of cells within a community can yield a strong ecological advantage. This is a key factor underlying the diverse origins of multicellularity.

No MeSH data available.


Related in: MedlinePlus