Chapter 4 : Division of Labor in Biofilms: the Ecology of Cell Differentiation

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One of the most remarkable features of the evolutionary process is its capacity to construct. In billions of years a primordial soup of organic compounds evolved to the theater of life extant today. This ability to construct is best illustrated by a number of transitions that have occurred during the natural history of our planet, such as the evolution of the first prebiotic cells, eukaryotes, multicellularity, and eusociality ( ). These transitions all bear a number of striking similarities ( ). First, construction evolves through cooperation ( ). That is, new organizational layers come about through the cooperative interaction of biological units that previously functioned independently. For example, organelles evolved from microbes that engaged in mutualistic interactions through endosymbiosis, and multicellularity evolved from cells that cooperate by sticking together, either via incomplete cell division or through aggregation ( ). In addition to cooperation, a second aspect characterizes major evolutionary transitions: the division of labor ( ). A precise definition of the division of labor will be given below, but one can loosely speak of division of labor when individuals—during their cooperative interactions—specialize in performing different “tasks.” Perhaps the most striking example comes from multicellular development. Multicellular organisms consist of many specialized cell types (e.g., muscle cells, neurons, epithelia, etc.). Despite being genetically identical, these cells have differentiated and thereby organized themselves in different physiological and morphological structures (e.g., organs) that together make up the individual.

Citation: van Gestel J, Vlamakis H, Kolter R. 2015. Division of Labor in Biofilms: the Ecology of Cell Differentiation, p 67-97. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0002-2014
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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.

Citation: van Gestel J, Vlamakis H, Kolter R. 2015. Division of Labor in Biofilms: the Ecology of Cell Differentiation, p 67-97. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. 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.

Citation: van Gestel J, Vlamakis H, Kolter R. 2015. Division of Labor in Biofilms: the Ecology of Cell Differentiation, p 67-97. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. 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.

Citation: van Gestel J, Vlamakis H, Kolter R. 2015. Division of Labor in Biofilms: the Ecology of Cell Differentiation, p 67-97. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0002-2014
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Figure 4

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 and .

Citation: van Gestel J, Vlamakis H, Kolter R. 2015. Division of Labor in Biofilms: the Ecology of Cell Differentiation, p 67-97. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. 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 , and .

Citation: van Gestel J, Vlamakis H, Kolter R. 2015. Division of Labor in Biofilms: the Ecology of Cell Differentiation, p 67-97. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. 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.

Citation: van Gestel J, Vlamakis H, Kolter R. 2015. Division of Labor in Biofilms: the Ecology of Cell Differentiation, p 67-97. In Ghannoum M, Parsek M, Whiteley M, Mukherjee P (ed), Microbial Biofilms, Second Edition. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MB-0002-2014
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