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Ecological perspectives on synthetic biology: insights from microbial population biology.

Escalante AE, Rebolleda-Gómez M, Benítez M, Travisano M - Front Microbiol (2015)

Bottom Line: In particular, we focus on the combined effect of spatial structure (connectivity of molecules and cells within the system) and ecological interactions (reciprocal and non-reciprocal) on the persistence of microbial consortia.We discuss exemplary cases to illustrate these ideas from published studies in evolutionary biology and biotechnology.We conclude by making clear the relevance of incorporating evolutionary and ecological principles to the design of microbial consortia, as a way of achieving evolutionarily stable and sustainable systems.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology, Evolution and Behavior, University of Minnesota St. Paul, MN, USA ; Laboratorio Nacional de Ciencias de la Sostenibilidad, Departamento de Ecología de la Biodiversidad Instituto de Ecología, Universidad Nacional Autónoma de México Mexico City, Mexico.

ABSTRACT
The metabolic capabilities of microbes are the basis for many major biotechnological advances, exploiting microbial diversity by selection or engineering of single strains. However, there are limits to the advances that can be achieved with single strains, and attention has turned toward the metabolic potential of consortia and the field of synthetic ecology. The main challenge for the synthetic ecology is that consortia are frequently unstable, largely because evolution by constituent members affects their interactions, which are the basis of collective metabolic functionality. Current practices in modeling consortia largely consider interactions as fixed circuits of chemical reactions, which greatly increases their tractability. This simplification comes at the cost of essential biological realism, stripping out the ecological context in which the metabolic actions occur and the potential for evolutionary change. In other words, evolutionary stability is not engineered into the system. This realization highlights the necessity to better identify the key components that influence the stable coexistence of microorganisms. Inclusion of ecological and evolutionary principles, in addition to biophysical variables and stoichiometric modeling of metabolism, is critical for microbial consortia design. This review aims to bring ecological and evolutionary concepts to the discussion on the stability of microbial consortia. In particular, we focus on the combined effect of spatial structure (connectivity of molecules and cells within the system) and ecological interactions (reciprocal and non-reciprocal) on the persistence of microbial consortia. We discuss exemplary cases to illustrate these ideas from published studies in evolutionary biology and biotechnology. We conclude by making clear the relevance of incorporating evolutionary and ecological principles to the design of microbial consortia, as a way of achieving evolutionarily stable and sustainable systems.

No MeSH data available.


Related in: MedlinePlus

Ecological dynamics and potential evolutionary outcomes of engineered cooperative consortia. In the left column are stable short-term dynamics; the right column, illustrates long-term outcomes if cheaters arose by mutation. (A) Two populations with strict interdependence by the production of essential aminoacids (one strain produces the aminoacid that the other cannot and vice versa). The release of the specific metabolic product is associated with near cell death of the producer and the decline of population density, producing population oscillatory dynamics. Over longer periods of time, cheaters can appear in the population, obtaining the benefits without paying the associated costs, and in the absence of spatial structure cheaters can spread leading to the collapse of the system (example from Shou et al., 2007). (B) A microbial consortium produces fluorescence as a cooperative trait regulated by a mechanism of consensus quorum sensing (QS). The signal molecules of this QS mechanism act as positive feedback between the two populations of cells for the production of both fluorescence and more signal molecules. The ecological role of each population is not described but cheaters can arise and disrupt the system, impeding fluorescence production (example from Brenner et al., 2007). (C) Reciprocal interaction circuit where two populations of cells are maintained in culture. One of the populations provides essential components to the other through volatile signals or direct transfer of medium, this system is thus open to the evolution of cheaters and collapse of the system. System collapse could potentially be prevented by including a redundancy component and local extinction and migration (metapopulation structure) via the replacement of populations in which cheaters appear with populations in which cheaters are absent (example from Weber et al., 2007).
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Figure 3: Ecological dynamics and potential evolutionary outcomes of engineered cooperative consortia. In the left column are stable short-term dynamics; the right column, illustrates long-term outcomes if cheaters arose by mutation. (A) Two populations with strict interdependence by the production of essential aminoacids (one strain produces the aminoacid that the other cannot and vice versa). The release of the specific metabolic product is associated with near cell death of the producer and the decline of population density, producing population oscillatory dynamics. Over longer periods of time, cheaters can appear in the population, obtaining the benefits without paying the associated costs, and in the absence of spatial structure cheaters can spread leading to the collapse of the system (example from Shou et al., 2007). (B) A microbial consortium produces fluorescence as a cooperative trait regulated by a mechanism of consensus quorum sensing (QS). The signal molecules of this QS mechanism act as positive feedback between the two populations of cells for the production of both fluorescence and more signal molecules. The ecological role of each population is not described but cheaters can arise and disrupt the system, impeding fluorescence production (example from Brenner et al., 2007). (C) Reciprocal interaction circuit where two populations of cells are maintained in culture. One of the populations provides essential components to the other through volatile signals or direct transfer of medium, this system is thus open to the evolution of cheaters and collapse of the system. System collapse could potentially be prevented by including a redundancy component and local extinction and migration (metapopulation structure) via the replacement of populations in which cheaters appear with populations in which cheaters are absent (example from Weber et al., 2007).

Mentions: Work by Shou et al. (2007) is a good example of how engineered consortia can be better understood and designed, if simple ecological and evolutionary principles are taken into consideration. The system was designed taking into account ecological feedbacks (reciprocal interaction), consisting of two engineered yeast genotypes that were cultured with no explicit reference to any spatial structure in liquid media. Each genotype was auxotrophic for a specific amino acid that was overproduced by the other genotype. This strict dependence on the production of essential amino acids generated frequency-dependent selection that stabilized the community. In this system, a genotype increases in frequency when it is rare due to the abundance of its growth limiting essential amino acid. In contrast, the more common genotype decreases in frequency because of the scarcity of its growth limiting amino acid, which is produced by the rare genotype (Figure 3A).


Ecological perspectives on synthetic biology: insights from microbial population biology.

Escalante AE, Rebolleda-Gómez M, Benítez M, Travisano M - Front Microbiol (2015)

Ecological dynamics and potential evolutionary outcomes of engineered cooperative consortia. In the left column are stable short-term dynamics; the right column, illustrates long-term outcomes if cheaters arose by mutation. (A) Two populations with strict interdependence by the production of essential aminoacids (one strain produces the aminoacid that the other cannot and vice versa). The release of the specific metabolic product is associated with near cell death of the producer and the decline of population density, producing population oscillatory dynamics. Over longer periods of time, cheaters can appear in the population, obtaining the benefits without paying the associated costs, and in the absence of spatial structure cheaters can spread leading to the collapse of the system (example from Shou et al., 2007). (B) A microbial consortium produces fluorescence as a cooperative trait regulated by a mechanism of consensus quorum sensing (QS). The signal molecules of this QS mechanism act as positive feedback between the two populations of cells for the production of both fluorescence and more signal molecules. The ecological role of each population is not described but cheaters can arise and disrupt the system, impeding fluorescence production (example from Brenner et al., 2007). (C) Reciprocal interaction circuit where two populations of cells are maintained in culture. One of the populations provides essential components to the other through volatile signals or direct transfer of medium, this system is thus open to the evolution of cheaters and collapse of the system. System collapse could potentially be prevented by including a redundancy component and local extinction and migration (metapopulation structure) via the replacement of populations in which cheaters appear with populations in which cheaters are absent (example from Weber et al., 2007).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4341553&req=5

Figure 3: Ecological dynamics and potential evolutionary outcomes of engineered cooperative consortia. In the left column are stable short-term dynamics; the right column, illustrates long-term outcomes if cheaters arose by mutation. (A) Two populations with strict interdependence by the production of essential aminoacids (one strain produces the aminoacid that the other cannot and vice versa). The release of the specific metabolic product is associated with near cell death of the producer and the decline of population density, producing population oscillatory dynamics. Over longer periods of time, cheaters can appear in the population, obtaining the benefits without paying the associated costs, and in the absence of spatial structure cheaters can spread leading to the collapse of the system (example from Shou et al., 2007). (B) A microbial consortium produces fluorescence as a cooperative trait regulated by a mechanism of consensus quorum sensing (QS). The signal molecules of this QS mechanism act as positive feedback between the two populations of cells for the production of both fluorescence and more signal molecules. The ecological role of each population is not described but cheaters can arise and disrupt the system, impeding fluorescence production (example from Brenner et al., 2007). (C) Reciprocal interaction circuit where two populations of cells are maintained in culture. One of the populations provides essential components to the other through volatile signals or direct transfer of medium, this system is thus open to the evolution of cheaters and collapse of the system. System collapse could potentially be prevented by including a redundancy component and local extinction and migration (metapopulation structure) via the replacement of populations in which cheaters appear with populations in which cheaters are absent (example from Weber et al., 2007).
Mentions: Work by Shou et al. (2007) is a good example of how engineered consortia can be better understood and designed, if simple ecological and evolutionary principles are taken into consideration. The system was designed taking into account ecological feedbacks (reciprocal interaction), consisting of two engineered yeast genotypes that were cultured with no explicit reference to any spatial structure in liquid media. Each genotype was auxotrophic for a specific amino acid that was overproduced by the other genotype. This strict dependence on the production of essential amino acids generated frequency-dependent selection that stabilized the community. In this system, a genotype increases in frequency when it is rare due to the abundance of its growth limiting essential amino acid. In contrast, the more common genotype decreases in frequency because of the scarcity of its growth limiting amino acid, which is produced by the rare genotype (Figure 3A).

Bottom Line: In particular, we focus on the combined effect of spatial structure (connectivity of molecules and cells within the system) and ecological interactions (reciprocal and non-reciprocal) on the persistence of microbial consortia.We discuss exemplary cases to illustrate these ideas from published studies in evolutionary biology and biotechnology.We conclude by making clear the relevance of incorporating evolutionary and ecological principles to the design of microbial consortia, as a way of achieving evolutionarily stable and sustainable systems.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology, Evolution and Behavior, University of Minnesota St. Paul, MN, USA ; Laboratorio Nacional de Ciencias de la Sostenibilidad, Departamento de Ecología de la Biodiversidad Instituto de Ecología, Universidad Nacional Autónoma de México Mexico City, Mexico.

ABSTRACT
The metabolic capabilities of microbes are the basis for many major biotechnological advances, exploiting microbial diversity by selection or engineering of single strains. However, there are limits to the advances that can be achieved with single strains, and attention has turned toward the metabolic potential of consortia and the field of synthetic ecology. The main challenge for the synthetic ecology is that consortia are frequently unstable, largely because evolution by constituent members affects their interactions, which are the basis of collective metabolic functionality. Current practices in modeling consortia largely consider interactions as fixed circuits of chemical reactions, which greatly increases their tractability. This simplification comes at the cost of essential biological realism, stripping out the ecological context in which the metabolic actions occur and the potential for evolutionary change. In other words, evolutionary stability is not engineered into the system. This realization highlights the necessity to better identify the key components that influence the stable coexistence of microorganisms. Inclusion of ecological and evolutionary principles, in addition to biophysical variables and stoichiometric modeling of metabolism, is critical for microbial consortia design. This review aims to bring ecological and evolutionary concepts to the discussion on the stability of microbial consortia. In particular, we focus on the combined effect of spatial structure (connectivity of molecules and cells within the system) and ecological interactions (reciprocal and non-reciprocal) on the persistence of microbial consortia. We discuss exemplary cases to illustrate these ideas from published studies in evolutionary biology and biotechnology. We conclude by making clear the relevance of incorporating evolutionary and ecological principles to the design of microbial consortia, as a way of achieving evolutionarily stable and sustainable systems.

No MeSH data available.


Related in: MedlinePlus