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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

Colony expansion in wild type and biofilm-related mutants.Left: time course experiment of colony growth in WT and colony expansion in srfA, tasA, eps, sigF, and hag mutants, which are defective in producing surfactin, TasA, EPS, sporulation, and motility, respectively. Colonies are toothpick inoculated onto MSggN medium as described in the Materials and Methods. Right: WT colony after 70 h. The different regions of the colony are named: dendrites, petals, and rays.
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pbio.1002141.g001: Colony expansion in wild type and biofilm-related mutants.Left: time course experiment of colony growth in WT and colony expansion in srfA, tasA, eps, sigF, and hag mutants, which are defective in producing surfactin, TasA, EPS, sporulation, and motility, respectively. Colonies are toothpick inoculated onto MSggN medium as described in the Materials and Methods. Right: WT colony after 70 h. The different regions of the colony are named: dendrites, petals, and rays.

Mentions: We studied migration by examining colony growth on MSggN [57]. MSggN is a growth medium that induces colony expansion and resembles the biofilm-inducing medium, MSgg, that is typically used to study cell differentiation in the context of B. subtilis biofilms [21,38,57]. Colony expansion is more apparent on MSggN than on MSgg, which makes the former more suitable for studying migration (see Materials and Methods). Colony growth on MSggN consists of two main phases that are morphologically distinct (Fig 1; see also [57]). First, the colony forms dendrites that spread radially from the inoculum. Second, phenotypically distinct outgrowths, which we call “petals,” appear at the end of the dendrites. In some instances the petals change into another morphological structure at the colony edge, which we call “rays.” The distinct growth phases do not result from genetic change, because cells from the morphologically distinct regions of the colony behave the same as wild type (WT) when re-inoculated onto a fresh growth medium (S1 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)

Colony expansion in wild type and biofilm-related mutants.Left: time course experiment of colony growth in WT and colony expansion in srfA, tasA, eps, sigF, and hag mutants, which are defective in producing surfactin, TasA, EPS, sporulation, and motility, respectively. Colonies are toothpick inoculated onto MSggN medium as described in the Materials and Methods. Right: WT colony after 70 h. The different regions of the colony are named: dendrites, petals, and rays.
© Copyright Policy
Related In: Results  -  Collection

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

pbio.1002141.g001: Colony expansion in wild type and biofilm-related mutants.Left: time course experiment of colony growth in WT and colony expansion in srfA, tasA, eps, sigF, and hag mutants, which are defective in producing surfactin, TasA, EPS, sporulation, and motility, respectively. Colonies are toothpick inoculated onto MSggN medium as described in the Materials and Methods. Right: WT colony after 70 h. The different regions of the colony are named: dendrites, petals, and rays.
Mentions: We studied migration by examining colony growth on MSggN [57]. MSggN is a growth medium that induces colony expansion and resembles the biofilm-inducing medium, MSgg, that is typically used to study cell differentiation in the context of B. subtilis biofilms [21,38,57]. Colony expansion is more apparent on MSggN than on MSgg, which makes the former more suitable for studying migration (see Materials and Methods). Colony growth on MSggN consists of two main phases that are morphologically distinct (Fig 1; see also [57]). First, the colony forms dendrites that spread radially from the inoculum. Second, phenotypically distinct outgrowths, which we call “petals,” appear at the end of the dendrites. In some instances the petals change into another morphological structure at the colony edge, which we call “rays.” The distinct growth phases do not result from genetic change, because cells from the morphologically distinct regions of the colony behave the same as wild type (WT) when re-inoculated onto a fresh growth medium (S1 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