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Division of Labor in Biofilms: the Ecology of Cell Differentiation

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  • Authors: Jordi van Gestel1, Hera Vlamakis2, Roberto Kolter3
  • Editors: Mahmoud Ghannoum4, Matthew Parsek5, Marvin Whiteley6, Pranab Mukherjee7
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA 02115; 2: Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA 02115; 3: Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA 02115; 4: Case Western Reserve University, Cleveland, OH; 5: University of Washington, Seattle, WA; 6: University of Texas at Austin, Austin, TX; 7: Case Western Reserve University, Cleveland, OH
  • Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MB-0002-2014
  • Received 07 March 2014 Accepted 12 August 2014 Published 03 April 2015
  • Roberto Kolter, rkolter@hms.harvard.edu
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  • Abstract:

    The dense aggregation of cells on a surface, as seen in biofilms, inevitably results in both environmental and cellular heterogeneity. For example, nutrient gradients can trigger cells to differentiate into various phenotypic states. Not only do cells adapt physiologically to the local environmental conditions, but they also differentiate into cell types that interact with each other. This allows for task differentiation and, hence, the division of labor. In this article, we focus on cell differentiation and the division of labor in three bacterial species: , and . During biofilm formation each of these species differentiates into distinct cell types, in some cases leading to cooperative interactions. The division of labor and the cooperative interactions between cell types are assumed to yield an emergent ecological benefit. Yet in most cases the ecological benefits have yet to be elucidated. A notable exception is , in which cell differentiation within fruiting bodies facilitates the dispersal of spores. We argue that the ecological benefits of the division of labor might best be understood when we consider the dynamic nature of both biofilm formation and degradation.

  • Citation: van Gestel J, Vlamakis H, Kolter R. 2015. Division of Labor in Biofilms: the Ecology of Cell Differentiation. Microbiol Spectrum 3(2):MB-0002-2014. doi:10.1128/microbiolspec.MB-0002-2014.

Key Concept Ranking

Programmed Cell Death
0.40930122
Confocal Laser Scanning Microscopy
0.40213883
0.40930122

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/content/journal/microbiolspec/10.1128/microbiolspec.MB-0002-2014
2015-04-03
2017-03-25

Abstract:

The dense aggregation of cells on a surface, as seen in biofilms, inevitably results in both environmental and cellular heterogeneity. For example, nutrient gradients can trigger cells to differentiate into various phenotypic states. Not only do cells adapt physiologically to the local environmental conditions, but they also differentiate into cell types that interact with each other. This allows for task differentiation and, hence, the division of labor. In this article, we focus on cell differentiation and the division of labor in three bacterial species: , and . During biofilm formation each of these species differentiates into distinct cell types, in some cases leading to cooperative interactions. The division of labor and the cooperative interactions between cell types are assumed to yield an emergent ecological benefit. Yet in most cases the ecological benefits have yet to be elucidated. A notable exception is , in which cell differentiation within fruiting bodies facilitates the dispersal of spores. We argue that the ecological benefits of the division of labor might best be understood when we consider the dynamic nature of both biofilm formation and degradation.

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FIGURE 1

Conceptual and theoretical basis for the division of labor. (A) Growth of cooperative and noncooperative cells when mixed (left) or segregated (right). When mixed, the noncooperative genotype performs better than the cooperative phenotype; it benefits from cooperation without paying the costs. When segregated, the cooperative genotype performs better. (B) Reaction norms. Different colored lines and associated numbers show different types of reaction norms as indicated on the right. (C) Fitness consequences of cell differentiation at the individual level (i.e., cell) and group level (i.e., colony or part of the colony). When cell differentiation is not beneficial at either level, phenotypic heterogeneity is nonadaptive. When it is only beneficial at the cell level, there is cellular specialization. When it is only beneficial at the colony level, there is division of labor. When it is beneficial at both levels, one cannot directly determine the function of cell differentiation. doi:10.1128/microbiolspec.MB-0002-2014.f1

Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MB-0002-2014
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FIGURE 2

Phenotypic trade-offs and the division of labor. Trade-off between two tasks: phenotype A and B. The trade-off constrains a cell such that expressing phenotype A (e.g., photosynthesis) is at the expense of phenotype B (e.g., nitrogen fixation). The trade-off can be weak (concave shape) or strong (convex shape). (A) Expected evolutionary outcome when the trade-off between phenotypes A and B is weak: phenotypic generalist. The regulatory network that controls the expression of phenotypes A and B should result in coexpression. (B) Expected evolutionary outcome when the trade-off between phenotypes A and B is strong: cell specialization and the division of labor. In this case, the regulatory network that controls the expression of phenotypes A and B should result in antagonistic expression and commit cells to a given cell type (positive feedback loops). Consequently, each cell expresses only phenotype A or B. doi:10.1128/microbiolspec.MB-0002-2014.f2

Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MB-0002-2014
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FIGURE 3

Bacterial multicellularity. For each form of multicellularity we show a number of different cell types: green is vegetative cells, blue is spores, and red is terminally differentiated cells, including cells that undergo lysis. (A) Filamentous multicellularity and cell differentiation in cyanobacteria. PatS is a signaling peptide that blocks heterocyst formation in the neighboring cells in the cyanobacteria filaments. (B) Filamentous multicellularity and aerial hyphae formation in actinobacteria. (C) Colonial multicellularity and fruiting body formation in myxobacteria. A-signal-dependent aggregation is illustrated by an arrow, and the level of C-signal is highest in the base and center of a fruiting body. doi:10.1128/microbiolspec.MB-0002-2014.f3

Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MB-0002-2014
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FIGURE 4a

Cell differentiation and pattern formation in biofilms. (A) Simplified scheme of the regulatory circuit that controls cell differentiation. Regulatory repression (red T-bars) or stimulation (green arrows) can involve both transcriptional regulation and (de)phosphorylation. The gray box shows the expected developmental transition in time throughout biofilm formation: motile cells differentiate to matrix-producing cells, which later sporulate. S and S are environmental signals that affect the sensory kinases KinA-E and DegS. (B) Pattern formation in cross-sections and top view of colony biofilms. Cell types shown in cross-sections are sporulating cells (artificially colored yellow or green), motile cells (blue), and matrix-producing cells (red). In the top view, sporulating cells are shown in green and colocalize with the biofilm wrinkles. (C) Feedback between cellular contingency and environmental conditionality. Images are adapted from references 144 and 169 . doi:10.1128/microbiolspec.MB-0002-2014.f4a

Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MB-0002-2014
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FIGURE 4b

Cell differentiation and pattern formation in biofilms. (A) Simplified scheme of the regulatory circuit that controls cell differentiation. Regulatory repression (red T-bars) or stimulation (green arrows) can involve both transcriptional regulation and (de)phosphorylation. The gray box shows the expected developmental transition in time throughout biofilm formation: motile cells differentiate to matrix-producing cells, which later sporulate. S and S are environmental signals that affect the sensory kinases KinA-E and DegS. (B) Pattern formation in cross-sections and top view of colony biofilms. Cell types shown in cross-sections are sporulating cells (artificially colored yellow or green), motile cells (blue), and matrix-producing cells (red). In the top view, sporulating cells are shown in green and colocalize with the biofilm wrinkles. (C) Feedback between cellular contingency and environmental conditionality. Images are adapted from references 144 and 169 . doi:10.1128/microbiolspec.MB-0002-2014.f4b

Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MB-0002-2014
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FIGURE 5

Pattern formation in microcolonies. (A) Fruiting bodies consisting of nonmotile stalk cells (blue) and motile cap cells (yellow). (B) Localization of eDNA in microcolonies (red). (C) Localization of rhamnolipid production (yellow). (D) Live (green) and dead (yellow/red) cells after EDTA treatment in a 4-day-old microcolony. (E) Schematic overview of mushroom-shaped microcolonies and the interaction between the stalk and cap cells through the production of the iron-scavenging siderophore pyoverdine. Images adapted from references 178 , 190 , 192 , and 196 . doi:10.1128/microbiolspec.MB-0002-2014.f5

Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MB-0002-2014
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FIGURE 6

Simplified schematic view of the life cycle of biofilm formation. The life cycle is divided into two life phases: the multicellular phase and the dispersal phase. Various environmental conditions influence the switch toward aggregation, typically mediated by a second messenger. When the second messenger passes a certain threshold, aggregation is initiated and, the other way around, when it drops below a certain threshold, cells revert to the dispersal phase. doi:10.1128/microbiolspec.MB-0002-2014.f6

Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MB-0002-2014
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