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An Economic Framework of Microbial Trade.

Tasoff J, Mee MT, Wang HH - PLoS ONE (2015)

Bottom Line: Our biotic GET (BGET) model provides an a priori theory of the growth benefits of microbial trade, yielding several novel insights relevant to understanding microbial ecology and engineering synthetic communities.Furthermore, we find that species engaged in trade exhibit a fundamental tradeoff between growth rate and relative population abundance, and that different environments that put greater pressure on group selection versus individual selection will promote varying strategies along this growth-abundance spectrum.This framework provides a foundation to study natural and engineered microbial communities through a new lens based on economic theories developed over the past century.

View Article: PubMed Central - PubMed

Affiliation: Department of Economics, Claremont Graduate University, Claremont, California, United States of America.

ABSTRACT
A large fraction of microbial life on earth exists in complex communities where metabolic exchange is vital. Microbes trade essential resources to promote their own growth in an analogous way to countries that exchange goods in modern economic markets. Inspired by these similarities, we developed a framework based on general equilibrium theory (GET) from economics to predict the population dynamics of trading microbial communities. Our biotic GET (BGET) model provides an a priori theory of the growth benefits of microbial trade, yielding several novel insights relevant to understanding microbial ecology and engineering synthetic communities. We find that the economic concept of comparative advantage is a necessary condition for mutualistic trade. Our model suggests that microbial communities can grow faster when species are unable to produce essential resources that are obtained through trade, thereby promoting metabolic specialization and increased intercellular exchange. Furthermore, we find that species engaged in trade exhibit a fundamental tradeoff between growth rate and relative population abundance, and that different environments that put greater pressure on group selection versus individual selection will promote varying strategies along this growth-abundance spectrum. We experimentally tested this tradeoff using a synthetic consortium of Escherichia coli cells and found the results match the predictions of the model. This framework provides a foundation to study natural and engineered microbial communities through a new lens based on economic theories developed over the past century.

No MeSH data available.


Related in: MedlinePlus

Production and consumption of a species-1 cell in a co-culture.(a) Population equilibrium under autarky (no trade). The blue arrow represents the direction of increasing utility. Consumption of the metabolites in the ratio  lead to growth. The indifference curves are contour lines of the utility function: any two consumption vectors on the same indifference curve lead to the same growth rate. The solid red line represents the possible production vectors of metabolite-1 and metabolite-2. The intersection of the blue arrow with the consumption-set line is the equilibrium consumption vector for which utility is maximized. When there is no trade the consumption and production sets are equivalent. The cell can only consume what it produces. (b) Schematic of cells under autarky. Arrows represent the flow of resources during production and consumption of red and blue metabolites. The arrow width illustrates the utilization of each pathway. The gear size indicates pathway productivity. Cells need to allocate more input resources to produce metabolites for which it has lower productivity, given that utilization requirements are about equal. (c) Population equilibrium under trade where the consumption set is expanded (solid red line). The consumption set line shifts upward by the amount species-1 imports from species-2, . The increased magnitude of the slope of the consumption set line indicates that a fraction of metabolite-1 produced is exported to species-2. The slope is given by . The new equilibrium consumption vector and utility level is greater under trade than autarky implying higher growth rates. (d) Schematic of trading cells. A cell can allocate most of its input resources to produce metabolites for which it has high productivity when exchange occurs.
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pone.0132907.g003: Production and consumption of a species-1 cell in a co-culture.(a) Population equilibrium under autarky (no trade). The blue arrow represents the direction of increasing utility. Consumption of the metabolites in the ratio lead to growth. The indifference curves are contour lines of the utility function: any two consumption vectors on the same indifference curve lead to the same growth rate. The solid red line represents the possible production vectors of metabolite-1 and metabolite-2. The intersection of the blue arrow with the consumption-set line is the equilibrium consumption vector for which utility is maximized. When there is no trade the consumption and production sets are equivalent. The cell can only consume what it produces. (b) Schematic of cells under autarky. Arrows represent the flow of resources during production and consumption of red and blue metabolites. The arrow width illustrates the utilization of each pathway. The gear size indicates pathway productivity. Cells need to allocate more input resources to produce metabolites for which it has lower productivity, given that utilization requirements are about equal. (c) Population equilibrium under trade where the consumption set is expanded (solid red line). The consumption set line shifts upward by the amount species-1 imports from species-2, . The increased magnitude of the slope of the consumption set line indicates that a fraction of metabolite-1 produced is exported to species-2. The slope is given by . The new equilibrium consumption vector and utility level is greater under trade than autarky implying higher growth rates. (d) Schematic of trading cells. A cell can allocate most of its input resources to produce metabolites for which it has high productivity when exchange occurs.

Mentions: The intuition for equilibrium can be expressed graphically (Fig 3). Under autarky (defined as no trade), the set of metabolites that could be produced is the same as the set that can be consumed. The cell adjusts production to obtain the maximum possible utility depicted by the intersection of the blue arrow and the red line (Fig 3A). If a cell of species-1 needs an equal amount of metabolite-1 and metabolite-2 for growth, and is more productive at generating metabolite 1, then the cell will devote relatively more input resources (e.g. glucose) to producing metabolite 2 (red arrows of Fig 3B). With trade, however, a cell of species-1 can receive metabolite-2 from species-2. Trade shifts the consumption set upwards by the amount of import, and it increases the magnitude of the slope of the consumption in proportion to the amount that the cell exports (Fig 3C). Thus, trade can increase the cell’s total consumption and hence increase its growth in a mutually beneficial fashion (Fig 3D).


An Economic Framework of Microbial Trade.

Tasoff J, Mee MT, Wang HH - PLoS ONE (2015)

Production and consumption of a species-1 cell in a co-culture.(a) Population equilibrium under autarky (no trade). The blue arrow represents the direction of increasing utility. Consumption of the metabolites in the ratio  lead to growth. The indifference curves are contour lines of the utility function: any two consumption vectors on the same indifference curve lead to the same growth rate. The solid red line represents the possible production vectors of metabolite-1 and metabolite-2. The intersection of the blue arrow with the consumption-set line is the equilibrium consumption vector for which utility is maximized. When there is no trade the consumption and production sets are equivalent. The cell can only consume what it produces. (b) Schematic of cells under autarky. Arrows represent the flow of resources during production and consumption of red and blue metabolites. The arrow width illustrates the utilization of each pathway. The gear size indicates pathway productivity. Cells need to allocate more input resources to produce metabolites for which it has lower productivity, given that utilization requirements are about equal. (c) Population equilibrium under trade where the consumption set is expanded (solid red line). The consumption set line shifts upward by the amount species-1 imports from species-2, . The increased magnitude of the slope of the consumption set line indicates that a fraction of metabolite-1 produced is exported to species-2. The slope is given by . The new equilibrium consumption vector and utility level is greater under trade than autarky implying higher growth rates. (d) Schematic of trading cells. A cell can allocate most of its input resources to produce metabolites for which it has high productivity when exchange occurs.
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getmorefigures.php?uid=PMC4519184&req=5

pone.0132907.g003: Production and consumption of a species-1 cell in a co-culture.(a) Population equilibrium under autarky (no trade). The blue arrow represents the direction of increasing utility. Consumption of the metabolites in the ratio lead to growth. The indifference curves are contour lines of the utility function: any two consumption vectors on the same indifference curve lead to the same growth rate. The solid red line represents the possible production vectors of metabolite-1 and metabolite-2. The intersection of the blue arrow with the consumption-set line is the equilibrium consumption vector for which utility is maximized. When there is no trade the consumption and production sets are equivalent. The cell can only consume what it produces. (b) Schematic of cells under autarky. Arrows represent the flow of resources during production and consumption of red and blue metabolites. The arrow width illustrates the utilization of each pathway. The gear size indicates pathway productivity. Cells need to allocate more input resources to produce metabolites for which it has lower productivity, given that utilization requirements are about equal. (c) Population equilibrium under trade where the consumption set is expanded (solid red line). The consumption set line shifts upward by the amount species-1 imports from species-2, . The increased magnitude of the slope of the consumption set line indicates that a fraction of metabolite-1 produced is exported to species-2. The slope is given by . The new equilibrium consumption vector and utility level is greater under trade than autarky implying higher growth rates. (d) Schematic of trading cells. A cell can allocate most of its input resources to produce metabolites for which it has high productivity when exchange occurs.
Mentions: The intuition for equilibrium can be expressed graphically (Fig 3). Under autarky (defined as no trade), the set of metabolites that could be produced is the same as the set that can be consumed. The cell adjusts production to obtain the maximum possible utility depicted by the intersection of the blue arrow and the red line (Fig 3A). If a cell of species-1 needs an equal amount of metabolite-1 and metabolite-2 for growth, and is more productive at generating metabolite 1, then the cell will devote relatively more input resources (e.g. glucose) to producing metabolite 2 (red arrows of Fig 3B). With trade, however, a cell of species-1 can receive metabolite-2 from species-2. Trade shifts the consumption set upwards by the amount of import, and it increases the magnitude of the slope of the consumption in proportion to the amount that the cell exports (Fig 3C). Thus, trade can increase the cell’s total consumption and hence increase its growth in a mutually beneficial fashion (Fig 3D).

Bottom Line: Our biotic GET (BGET) model provides an a priori theory of the growth benefits of microbial trade, yielding several novel insights relevant to understanding microbial ecology and engineering synthetic communities.Furthermore, we find that species engaged in trade exhibit a fundamental tradeoff between growth rate and relative population abundance, and that different environments that put greater pressure on group selection versus individual selection will promote varying strategies along this growth-abundance spectrum.This framework provides a foundation to study natural and engineered microbial communities through a new lens based on economic theories developed over the past century.

View Article: PubMed Central - PubMed

Affiliation: Department of Economics, Claremont Graduate University, Claremont, California, United States of America.

ABSTRACT
A large fraction of microbial life on earth exists in complex communities where metabolic exchange is vital. Microbes trade essential resources to promote their own growth in an analogous way to countries that exchange goods in modern economic markets. Inspired by these similarities, we developed a framework based on general equilibrium theory (GET) from economics to predict the population dynamics of trading microbial communities. Our biotic GET (BGET) model provides an a priori theory of the growth benefits of microbial trade, yielding several novel insights relevant to understanding microbial ecology and engineering synthetic communities. We find that the economic concept of comparative advantage is a necessary condition for mutualistic trade. Our model suggests that microbial communities can grow faster when species are unable to produce essential resources that are obtained through trade, thereby promoting metabolic specialization and increased intercellular exchange. Furthermore, we find that species engaged in trade exhibit a fundamental tradeoff between growth rate and relative population abundance, and that different environments that put greater pressure on group selection versus individual selection will promote varying strategies along this growth-abundance spectrum. We experimentally tested this tradeoff using a synthetic consortium of Escherichia coli cells and found the results match the predictions of the model. This framework provides a foundation to study natural and engineered microbial communities through a new lens based on economic theories developed over the past century.

No MeSH data available.


Related in: MedlinePlus