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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

Temporal gene expression dynamics of srfA and tapA during colony expansion in wild-type cells.Surfactin- and matrix-producing cells are monitored in a WT strain harboring promoter fusions (PsrfA-YFP and PtapA-CFP) of srfA and tapA to genes encoding yellow and cyan fluorescent proteins, respectively. (A) The average expression level of tapA and srfA was measured by microscopy 2, 4, 6, 8, 10, 12, 24, 31 h after inoculation. The average expression level is equal to the average fluorescence intensity in labeled WT cells (n = 20–50 microscopy images per time step) minus that in non-labeled WT cells (n = 10–30 microscopy images per time step). Fluorescence intensity data were acquired from segmented microscopy images (n = 439; containing many thousands of cells). (B) Representative microscopy images from colonies dissected at 10 h (1) and 31 h (2) after inoculation. AU, arbitrary units. Cells expressing srfA are false-colored red, and cells expressing tapA are false-colored green.
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pbio.1002141.g003: Temporal gene expression dynamics of srfA and tapA during colony expansion in wild-type cells.Surfactin- and matrix-producing cells are monitored in a WT strain harboring promoter fusions (PsrfA-YFP and PtapA-CFP) of srfA and tapA to genes encoding yellow and cyan fluorescent proteins, respectively. (A) The average expression level of tapA and srfA was measured by microscopy 2, 4, 6, 8, 10, 12, 24, 31 h after inoculation. The average expression level is equal to the average fluorescence intensity in labeled WT cells (n = 20–50 microscopy images per time step) minus that in non-labeled WT cells (n = 10–30 microscopy images per time step). Fluorescence intensity data were acquired from segmented microscopy images (n = 439; containing many thousands of cells). (B) Representative microscopy images from colonies dissected at 10 h (1) and 31 h (2) after inoculation. AU, arbitrary units. Cells expressing srfA are false-colored red, and cells expressing tapA are false-colored green.

Mentions: Fig 3A shows the expression of srfA and tapA over time. The expression pattern is characterized by two phases: in the first phase there is a peak in the average expression of srfA, while in the second phase there is sharp increase in the average expression of tapA (Fig 3A). Fig 3B shows a representative image from each of these two phases. At the onset of colony growth there is also a slight peak in tapA expression, which is due to background expression in the inoculation conditions (for details see Materials and Methods). When taking the time frame of gene expression into consideration, the up-regulation of srfA corresponds to dendrite formation, and the up-regulation of tapA corresponds to petal formation (Figs 1 and 3). The distinct growth phases that are apparent at the macroscopic level therefore relate to gene expression dynamics at the cell level (microscopic). The same microscopy images were used to examine the co-expression of srfA and tapA. As expected from previous studies [42], the expression of srfA and the expression of tapA were mutually exclusive (S1 Text; S2 Fig). This confirmed that also for our growth conditions, surfactin-producing and matrix-producing cells are mutually exclusive and distinct cell types (S2 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)

Temporal gene expression dynamics of srfA and tapA during colony expansion in wild-type cells.Surfactin- and matrix-producing cells are monitored in a WT strain harboring promoter fusions (PsrfA-YFP and PtapA-CFP) of srfA and tapA to genes encoding yellow and cyan fluorescent proteins, respectively. (A) The average expression level of tapA and srfA was measured by microscopy 2, 4, 6, 8, 10, 12, 24, 31 h after inoculation. The average expression level is equal to the average fluorescence intensity in labeled WT cells (n = 20–50 microscopy images per time step) minus that in non-labeled WT cells (n = 10–30 microscopy images per time step). Fluorescence intensity data were acquired from segmented microscopy images (n = 439; containing many thousands of cells). (B) Representative microscopy images from colonies dissected at 10 h (1) and 31 h (2) after inoculation. AU, arbitrary units. Cells expressing srfA are false-colored red, and cells expressing tapA are false-colored green.
© Copyright Policy
Related In: Results  -  Collection

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

pbio.1002141.g003: Temporal gene expression dynamics of srfA and tapA during colony expansion in wild-type cells.Surfactin- and matrix-producing cells are monitored in a WT strain harboring promoter fusions (PsrfA-YFP and PtapA-CFP) of srfA and tapA to genes encoding yellow and cyan fluorescent proteins, respectively. (A) The average expression level of tapA and srfA was measured by microscopy 2, 4, 6, 8, 10, 12, 24, 31 h after inoculation. The average expression level is equal to the average fluorescence intensity in labeled WT cells (n = 20–50 microscopy images per time step) minus that in non-labeled WT cells (n = 10–30 microscopy images per time step). Fluorescence intensity data were acquired from segmented microscopy images (n = 439; containing many thousands of cells). (B) Representative microscopy images from colonies dissected at 10 h (1) and 31 h (2) after inoculation. AU, arbitrary units. Cells expressing srfA are false-colored red, and cells expressing tapA are false-colored green.
Mentions: Fig 3A shows the expression of srfA and tapA over time. The expression pattern is characterized by two phases: in the first phase there is a peak in the average expression of srfA, while in the second phase there is sharp increase in the average expression of tapA (Fig 3A). Fig 3B shows a representative image from each of these two phases. At the onset of colony growth there is also a slight peak in tapA expression, which is due to background expression in the inoculation conditions (for details see Materials and Methods). When taking the time frame of gene expression into consideration, the up-regulation of srfA corresponds to dendrite formation, and the up-regulation of tapA corresponds to petal formation (Figs 1 and 3). The distinct growth phases that are apparent at the macroscopic level therefore relate to gene expression dynamics at the cell level (microscopic). The same microscopy images were used to examine the co-expression of srfA and tapA. As expected from previous studies [42], the expression of srfA and the expression of tapA were mutually exclusive (S1 Text; S2 Fig). This confirmed that also for our growth conditions, surfactin-producing and matrix-producing cells are mutually exclusive and distinct cell types (S2 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