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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 chimeric colonies of sliding-deficient mutants.(A) Chimeric colonies of different pairwise combinations of sliding-deficient mutants (imaged 52 h after inoculation). Strains were mixed 1:1, and 2 μl of the mix was spotted in the center of the plate. (B) Colony expansion of eps tasA + srfA chimeras when inoculated in different ratios of eps tasA:srfA (imaged after 24 h): 9:1, 4:1, 1:1, 1:4, and 1:9. (C) Colony expansion of eps tasA–YFP (false-colored green) + WT-mKate2 (colored red; see S1 Table for specifications) chimeras for different initial ratios of eps tasA:WT (imaged after 32 h): 19:1, 9:1, and 1:1. Yellowish regions in the colony correspond to colony parts where both eps tasA and WT cells occur. In the rightmost fluorescence image, only the colony edge is shown, as the colony was too big for a single microscopy image (the center of this colony is towards the lower left corner). Images were taken with a stereomicroscope.
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pbio.1002141.g002: Colony expansion in chimeric colonies of sliding-deficient mutants.(A) Chimeric colonies of different pairwise combinations of sliding-deficient mutants (imaged 52 h after inoculation). Strains were mixed 1:1, and 2 μl of the mix was spotted in the center of the plate. (B) Colony expansion of eps tasA + srfA chimeras when inoculated in different ratios of eps tasA:srfA (imaged after 24 h): 9:1, 4:1, 1:1, 1:4, and 1:9. (C) Colony expansion of eps tasA–YFP (false-colored green) + WT-mKate2 (colored red; see S1 Table for specifications) chimeras for different initial ratios of eps tasA:WT (imaged after 32 h): 19:1, 9:1, and 1:1. Yellowish regions in the colony correspond to colony parts where both eps tasA and WT cells occur. In the rightmost fluorescence image, only the colony edge is shown, as the colony was too big for a single microscopy image (the center of this colony is towards the lower left corner). Images were taken with a stereomicroscope.

Mentions: To examine whether colony expansion could be recovered by extracellular complementation, different pairs of expansion-deficient mutants were cocultured as chimeric colonies [60]. Such two-mutant cocultures can reveal something about the interactions between different cell types during colony growth [45,61]. All examined chimeric colonies in which mutant cells were mixed at a 1:1 ratio showed a partial to full recovery of colony expansion when compared to the WT (Fig 2A). Interestingly, two of the chimeric colonies appeared to outperform WT in the extent of colony expansion: srfA + eps and eps tasA + srfA. Thus, the task differentiation of matrix and surfactin production by mutant strains enhanced the degree of colony expansion.


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 chimeric colonies of sliding-deficient mutants.(A) Chimeric colonies of different pairwise combinations of sliding-deficient mutants (imaged 52 h after inoculation). Strains were mixed 1:1, and 2 μl of the mix was spotted in the center of the plate. (B) Colony expansion of eps tasA + srfA chimeras when inoculated in different ratios of eps tasA:srfA (imaged after 24 h): 9:1, 4:1, 1:1, 1:4, and 1:9. (C) Colony expansion of eps tasA–YFP (false-colored green) + WT-mKate2 (colored red; see S1 Table for specifications) chimeras for different initial ratios of eps tasA:WT (imaged after 32 h): 19:1, 9:1, and 1:1. Yellowish regions in the colony correspond to colony parts where both eps tasA and WT cells occur. In the rightmost fluorescence image, only the colony edge is shown, as the colony was too big for a single microscopy image (the center of this colony is towards the lower left corner). Images were taken with a stereomicroscope.
© Copyright Policy
Related In: Results  -  Collection

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

pbio.1002141.g002: Colony expansion in chimeric colonies of sliding-deficient mutants.(A) Chimeric colonies of different pairwise combinations of sliding-deficient mutants (imaged 52 h after inoculation). Strains were mixed 1:1, and 2 μl of the mix was spotted in the center of the plate. (B) Colony expansion of eps tasA + srfA chimeras when inoculated in different ratios of eps tasA:srfA (imaged after 24 h): 9:1, 4:1, 1:1, 1:4, and 1:9. (C) Colony expansion of eps tasA–YFP (false-colored green) + WT-mKate2 (colored red; see S1 Table for specifications) chimeras for different initial ratios of eps tasA:WT (imaged after 32 h): 19:1, 9:1, and 1:1. Yellowish regions in the colony correspond to colony parts where both eps tasA and WT cells occur. In the rightmost fluorescence image, only the colony edge is shown, as the colony was too big for a single microscopy image (the center of this colony is towards the lower left corner). Images were taken with a stereomicroscope.
Mentions: To examine whether colony expansion could be recovered by extracellular complementation, different pairs of expansion-deficient mutants were cocultured as chimeric colonies [60]. Such two-mutant cocultures can reveal something about the interactions between different cell types during colony growth [45,61]. All examined chimeric colonies in which mutant cells were mixed at a 1:1 ratio showed a partial to full recovery of colony expansion when compared to the WT (Fig 2A). Interestingly, two of the chimeric colonies appeared to outperform WT in the extent of colony expansion: srfA + eps and eps tasA + srfA. Thus, the task differentiation of matrix and surfactin production by mutant strains enhanced the degree of colony expansion.

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