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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

Van Gogh bundles and colony edge for different mutants.The upper row of images shows colonies 18 h after inoculation. The middle row of images shows the presence or absence of loops at the colony edge. The lower row of images shows the presence or absence of van Gogh bundles at the colony edge. In total, five strains were examined, WT and four sliding-deficient mutants: srfA, eps, eps tasA, and tasA. Scale bars are identical for all images in a row.
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pbio.1002141.g009: Van Gogh bundles and colony edge for different mutants.The upper row of images shows colonies 18 h after inoculation. The middle row of images shows the presence or absence of loops at the colony edge. The lower row of images shows the presence or absence of van Gogh bundles at the colony edge. In total, five strains were examined, WT and four sliding-deficient mutants: srfA, eps, eps tasA, and tasA. Scale bars are identical for all images in a row.

Mentions: The lack of colony expansion in sliding-deficient mutants, with the exception of tasA, can be explained by the lack of van Gogh bundles and the associated loops at the colony edge (Fig 9). Interestingly, eps and eps tasA mutants do show chains of cells, similar to the chains of cells in van Gogh bundles, but they are not aligned with each other (Fig 9). The tasA mutant strain is mainly deficient in colony expansion during the second growth phase, as it can form dendrites (Fig 9). Furthermore, the filamentous loops at the edge of the tasA colony are typically smaller and show more folds than those of the WT (S13 Fig). We hypothesize that TasA, although not strictly required for the formation of van Gogh bundles, may fine-tune the folding properties of the bundles. This hypothesis is supported by the fact that TasA localizes to the pole-to-pole contact points between cells in the van Gogh bundles, where it potentially affects biophysical properties such as the bending rigidity (Fig 7). Interestingly, while the lack of TasA reduces colony expansion, the artificial overproduction of TasA does not enhance colony expansion (S14 Fig).


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

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

Van Gogh bundles and colony edge for different mutants.The upper row of images shows colonies 18 h after inoculation. The middle row of images shows the presence or absence of loops at the colony edge. The lower row of images shows the presence or absence of van Gogh bundles at the colony edge. In total, five strains were examined, WT and four sliding-deficient mutants: srfA, eps, eps tasA, and tasA. Scale bars are identical for all images in a row.
© Copyright Policy
Related In: Results  -  Collection

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

pbio.1002141.g009: Van Gogh bundles and colony edge for different mutants.The upper row of images shows colonies 18 h after inoculation. The middle row of images shows the presence or absence of loops at the colony edge. The lower row of images shows the presence or absence of van Gogh bundles at the colony edge. In total, five strains were examined, WT and four sliding-deficient mutants: srfA, eps, eps tasA, and tasA. Scale bars are identical for all images in a row.
Mentions: The lack of colony expansion in sliding-deficient mutants, with the exception of tasA, can be explained by the lack of van Gogh bundles and the associated loops at the colony edge (Fig 9). Interestingly, eps and eps tasA mutants do show chains of cells, similar to the chains of cells in van Gogh bundles, but they are not aligned with each other (Fig 9). The tasA mutant strain is mainly deficient in colony expansion during the second growth phase, as it can form dendrites (Fig 9). Furthermore, the filamentous loops at the edge of the tasA colony are typically smaller and show more folds than those of the WT (S13 Fig). We hypothesize that TasA, although not strictly required for the formation of van Gogh bundles, may fine-tune the folding properties of the bundles. This hypothesis is supported by the fact that TasA localizes to the pole-to-pole contact points between cells in the van Gogh bundles, where it potentially affects biophysical properties such as the bending rigidity (Fig 7). Interestingly, while the lack of TasA reduces colony expansion, the artificial overproduction of TasA does not enhance colony expansion (S14 Fig).

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