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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

Schematic overview of cell differentiation and collective properties in B. subtilis colony expansion.Red and green cells represent, respectively, surfactin- and matrix-producing cells. Dendrites predominantly consist of surfactin-producing cells interspersed with clumps of matrix-producing cells. The petals of the colony consist predominantly of matrix-producing cells that form van Gogh bundles. We propose that surfactin mediates the expansion of van Gogh bundles by reducing the friction between the van Gogh bundles and substrate and that van Gogh bundle expansion is driven by cell division. The elastic and folding properties—dependent on matrix-producing cells—of the van Gogh bundles allow for an efficient colony expansion and prevent the bundles from breaking under increased compression.
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pbio.1002141.g011: Schematic overview of cell differentiation and collective properties in B. subtilis colony expansion.Red and green cells represent, respectively, surfactin- and matrix-producing cells. Dendrites predominantly consist of surfactin-producing cells interspersed with clumps of matrix-producing cells. The petals of the colony consist predominantly of matrix-producing cells that form van Gogh bundles. We propose that surfactin mediates the expansion of van Gogh bundles by reducing the friction between the van Gogh bundles and substrate and that van Gogh bundle expansion is driven by cell division. The elastic and folding properties—dependent on matrix-producing cells—of the van Gogh bundles allow for an efficient colony expansion and prevent the bundles from breaking under increased compression.

Mentions: In this study we analyzed sliding motility in B. subtilis to determine the factors that allow for the collective migration of cells. We found that cells organize themselves into bundles that spread by forming expanding filamentous loops at the colony edge. These cell collectives, which we call van Gogh bundles, are distinct from previously described filaments in B. subtilis due to their strong alignment and functionality [21,67]. The folding properties of the filamentous loops determine the migration rate and, in part, depend on the products secreted by matrix-producing cells. The development and expansion of van Gogh bundles depend critically on the synergic interaction of surfactin-producing and matrix-producing cells. To our knowledge, this is the first example of bacterial cells dividing labor in order to overcome one of the major ecological challenges: migration (Fig 11).


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

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

Schematic overview of cell differentiation and collective properties in B. subtilis colony expansion.Red and green cells represent, respectively, surfactin- and matrix-producing cells. Dendrites predominantly consist of surfactin-producing cells interspersed with clumps of matrix-producing cells. The petals of the colony consist predominantly of matrix-producing cells that form van Gogh bundles. We propose that surfactin mediates the expansion of van Gogh bundles by reducing the friction between the van Gogh bundles and substrate and that van Gogh bundle expansion is driven by cell division. The elastic and folding properties—dependent on matrix-producing cells—of the van Gogh bundles allow for an efficient colony expansion and prevent the bundles from breaking under increased compression.
© Copyright Policy
Related In: Results  -  Collection

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

pbio.1002141.g011: Schematic overview of cell differentiation and collective properties in B. subtilis colony expansion.Red and green cells represent, respectively, surfactin- and matrix-producing cells. Dendrites predominantly consist of surfactin-producing cells interspersed with clumps of matrix-producing cells. The petals of the colony consist predominantly of matrix-producing cells that form van Gogh bundles. We propose that surfactin mediates the expansion of van Gogh bundles by reducing the friction between the van Gogh bundles and substrate and that van Gogh bundle expansion is driven by cell division. The elastic and folding properties—dependent on matrix-producing cells—of the van Gogh bundles allow for an efficient colony expansion and prevent the bundles from breaking under increased compression.
Mentions: In this study we analyzed sliding motility in B. subtilis to determine the factors that allow for the collective migration of cells. We found that cells organize themselves into bundles that spread by forming expanding filamentous loops at the colony edge. These cell collectives, which we call van Gogh bundles, are distinct from previously described filaments in B. subtilis due to their strong alignment and functionality [21,67]. The folding properties of the filamentous loops determine the migration rate and, in part, depend on the products secreted by matrix-producing cells. The development and expansion of van Gogh bundles depend critically on the synergic interaction of surfactin-producing and matrix-producing cells. To our knowledge, this is the first example of bacterial cells dividing labor in order to overcome one of the major ecological challenges: migration (Fig 11).

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