A synthetic differentiation circuit in Escherichia coli for suppressing mutant takeover

Differentiation is crucial for multicellularity. However, it is inherently susceptible to mutant cells that fail to differentiate. These mutants outcompete normal cells by excessive self-renewal. It remains unclear what mechanisms can resist such mutant expansion. Here, we demonstrate a solution by...

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Published inCell Vol. 187; no. 4; pp. 931 - 944.e12
Main Authors Glass, David S., Bren, Anat, Vaisbourd, Elizabeth, Mayo, Avi, Alon, Uri
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 15.02.2024
Cell Press
Subjects
differentiation
enzymes
Escherichia coli
evolution
fitness landscape engineering
multicellular consortia
mutants
progenitors
robustness
stem cell niche
stem cells
synthetic biology
synthetic development
synthetic multicellularity
transit-amplifying cells
synthetic biology
synthetic development
stem cells
progenitors
stem cell niche
differentiation
transit-amplifying cells
robustness
synthetic multicellularity
fitness landscape engineering
multicellular consortia
Online AccessGet full text
ISSN0092-8674
1097-4172
1097-4172
DOI10.1016/j.cell.2024.01.024

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Abstract Differentiation is crucial for multicellularity. However, it is inherently susceptible to mutant cells that fail to differentiate. These mutants outcompete normal cells by excessive self-renewal. It remains unclear what mechanisms can resist such mutant expansion. Here, we demonstrate a solution by engineering a synthetic differentiation circuit in Escherichia coli that selects against these mutants via a biphasic fitness strategy. The circuit provides tunable production of synthetic analogs of stem, progenitor, and differentiated cells. It resists mutations by coupling differentiation to the production of an essential enzyme, thereby disadvantaging non-differentiating mutants. The circuit selected for and maintained a positive differentiation rate in long-term evolution. Surprisingly, this rate remained constant across vast changes in growth conditions. We found that transit-amplifying cells (fast-growing progenitors) underlie this environmental robustness. Our results provide insight into the stability of differentiation and demonstrate a powerful method for engineering evolutionarily stable multicellular consortia. [Display omitted] •Synthetic E. coli differentiation produces a stem-progenitor-differentiated lineage•Cell-autonomous coupling to an essential trait suppresses differentiation mutants•Fast-growing progenitors provide environmentally robust biphasic differentiation•Fitness landscape engineering guides long-term, environmentally robust behavior Bacteria were engineered to produce analogs of stem, progenitor, and differentiated cells. Coupling differentiation to an essential trait generated a biphasic fitness landscape, suppressing mutant takeover and providing an environmentally robust differentiation rate.
AbstractList Differentiation is crucial for multicellularity. However, it is inherently susceptible to mutant cells that fail to differentiate. These mutants outcompete normal cells by excessive self-renewal. It remains unclear what mechanisms can resist such mutant expansion. Here, we demonstrate a solution by engineering a synthetic differentiation circuit in Escherichia coli that selects against these mutants via a biphasic fitness strategy. The circuit provides tunable production of synthetic analogs of stem, progenitor, and differentiated cells. It resists mutations by coupling differentiation to the production of an essential enzyme, thereby disadvantaging non-differentiating mutants. The circuit selected for and maintained a positive differentiation rate in long-term evolution. Surprisingly, this rate remained constant across vast changes in growth conditions. We found that transit-amplifying cells (fast-growing progenitors) underlie this environmental robustness. Our results provide insight into the stability of differentiation and demonstrate a powerful method for engineering evolutionarily stable multicellular consortia. [Display omitted] •Synthetic E. coli differentiation produces a stem-progenitor-differentiated lineage•Cell-autonomous coupling to an essential trait suppresses differentiation mutants•Fast-growing progenitors provide environmentally robust biphasic differentiation•Fitness landscape engineering guides long-term, environmentally robust behavior Bacteria were engineered to produce analogs of stem, progenitor, and differentiated cells. Coupling differentiation to an essential trait generated a biphasic fitness landscape, suppressing mutant takeover and providing an environmentally robust differentiation rate.
Differentiation is crucial for multicellularity. However, it is inherently susceptible to mutant cells that fail to differentiate. These mutants outcompete normal cells by excessive self-renewal. It remains unclear what mechanisms can resist such mutant expansion. Here, we demonstrate a solution by engineering a synthetic differentiation circuit in Escherichia coli that selects against these mutants via a biphasic fitness strategy. The circuit provides tunable production of synthetic analogs of stem, progenitor, and differentiated cells. It resists mutations by coupling differentiation to the production of an essential enzyme, thereby disadvantaging non-differentiating mutants. The circuit selected for and maintained a positive differentiation rate in long-term evolution. Surprisingly, this rate remained constant across vast changes in growth conditions. We found that transit-amplifying cells (fast-growing progenitors) underlie this environmental robustness. Our results provide insight into the stability of differentiation and demonstrate a powerful method for engineering evolutionarily stable multicellular consortia.Differentiation is crucial for multicellularity. However, it is inherently susceptible to mutant cells that fail to differentiate. These mutants outcompete normal cells by excessive self-renewal. It remains unclear what mechanisms can resist such mutant expansion. Here, we demonstrate a solution by engineering a synthetic differentiation circuit in Escherichia coli that selects against these mutants via a biphasic fitness strategy. The circuit provides tunable production of synthetic analogs of stem, progenitor, and differentiated cells. It resists mutations by coupling differentiation to the production of an essential enzyme, thereby disadvantaging non-differentiating mutants. The circuit selected for and maintained a positive differentiation rate in long-term evolution. Surprisingly, this rate remained constant across vast changes in growth conditions. We found that transit-amplifying cells (fast-growing progenitors) underlie this environmental robustness. Our results provide insight into the stability of differentiation and demonstrate a powerful method for engineering evolutionarily stable multicellular consortia.
Differentiation is crucial for multicellularity. However, it is inherently susceptible to mutant cells that fail to differentiate. These mutants outcompete normal cells by excessive self-renewal. It remains unclear what mechanisms can resist such mutant expansion. Here, we demonstrate a solution by engineering a synthetic differentiation circuit in Escherichia coli that selects against these mutants via a biphasic fitness strategy. The circuit provides tunable production of synthetic analogs of stem, progenitor, and differentiated cells. It resists mutations by coupling differentiation to the production of an essential enzyme, thereby disadvantaging non-differentiating mutants. The circuit selected for and maintained a positive differentiation rate in long-term evolution. Surprisingly, this rate remained constant across vast changes in growth conditions. We found that transit-amplifying cells (fast-growing progenitors) underlie this environmental robustness. Our results provide insight into the stability of differentiation and demonstrate a powerful method for engineering evolutionarily stable multicellular consortia.
Differentiation is crucial for multicellularity. However, it is inherently susceptible to mutant cells that fail to differentiate. These mutants outcompete normal cells by excessive self-renewal. It remains unclear what mechanisms can resist such mutant expansion. Here, we demonstrate a solution by engineering a synthetic differentiation circuit in Escherichia coli that selects against these mutants via a biphasic fitness strategy. The circuit provides tunable production of synthetic analogs of stem, progenitor, and differentiated cells. It resists mutations by coupling differentiation to the production of an essential enzyme, thereby disadvantaging non-differentiating mutants. The circuit selected for and maintained a positive differentiation rate in long-term evolution. Surprisingly, this rate remained constant across vast changes in growth conditions. We found that transit-amplifying cells (fast-growing progenitors) underlie this environmental robustness. Our results provide insight into the stability of differentiation and demonstrate a powerful method for engineering evolutionarily stable multicellular consortia. • Synthetic E. coli differentiation produces a stem-progenitor-differentiated lineage • Cell-autonomous coupling to an essential trait suppresses differentiation mutants • Fast-growing progenitors provide environmentally robust biphasic differentiation • Fitness landscape engineering guides long-term, environmentally robust behavior Bacteria were engineered to produce analogs of stem, progenitor, and differentiated cells. Coupling differentiation to an essential trait generated a biphasic fitness landscape, suppressing mutant takeover and providing an environmentally robust differentiation rate.
Author Mayo, Avi
Vaisbourd, Elizabeth
Bren, Anat
Glass, David S.
Alon, Uri
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Issue 4
Keywords synthetic biology
synthetic development
stem cells
progenitors
stem cell niche
differentiation
transit-amplifying cells
robustness
synthetic multicellularity
fitness landscape engineering
multicellular consortia
Language English
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Snippet Differentiation is crucial for multicellularity. However, it is inherently susceptible to mutant cells that fail to differentiate. These mutants outcompete...
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SubjectTerms differentiation
enzymes
Escherichia coli
evolution
fitness landscape engineering
multicellular consortia
mutants
progenitors
robustness
stem cell niche
stem cells
synthetic biology
synthetic development
synthetic multicellularity
transit-amplifying cells
Title A synthetic differentiation circuit in Escherichia coli for suppressing mutant takeover
URI https://dx.doi.org/10.1016/j.cell.2024.01.024
https://www.ncbi.nlm.nih.gov/pubmed/38320549
https://www.proquest.com/docview/2923323657
https://www.proquest.com/docview/3153807430
https://pubmed.ncbi.nlm.nih.gov/PMC10882425
Volume 187
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