Non‐genetic diversity modulates population performance

Abstract Biological functions are typically performed by groups of cells that express predominantly the same genes, yet display a continuum of phenotypes. While it is known how one genotype can generate such non‐genetic diversity, it remains unclear how different phenotypes contribute to the perform...

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Main Authors: Adam James Waite, Nicholas W Frankel, Yann S Dufour, Jessica F Johnston, Junjiajia Long, Thierry Emonet
Format: Article
Language:English
Published: Springer Nature 2016-12-01
Series:Molecular Systems Biology
Subjects:
Online Access:https://doi.org/10.15252/msb.20167044
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author Adam James Waite
Nicholas W Frankel
Yann S Dufour
Jessica F Johnston
Junjiajia Long
Thierry Emonet
author_facet Adam James Waite
Nicholas W Frankel
Yann S Dufour
Jessica F Johnston
Junjiajia Long
Thierry Emonet
author_sort Adam James Waite
collection DOAJ
description Abstract Biological functions are typically performed by groups of cells that express predominantly the same genes, yet display a continuum of phenotypes. While it is known how one genotype can generate such non‐genetic diversity, it remains unclear how different phenotypes contribute to the performance of biological function at the population level. We developed a microfluidic device to simultaneously measure the phenotype and chemotactic performance of tens of thousands of individual, freely swimming Escherichia coli as they climbed a gradient of attractant. We discovered that spatial structure spontaneously emerged from initially well‐mixed wild‐type populations due to non‐genetic diversity. By manipulating the expression of key chemotaxis proteins, we established a causal relationship between protein expression, non‐genetic diversity, and performance that was theoretically predicted. This approach generated a complete phenotype‐to‐performance map, in which we found a nonlinear regime. We used this map to demonstrate how changing the shape of a phenotypic distribution can have as large of an effect on collective performance as changing the mean phenotype, suggesting that selection could act on both during the process of adaptation.
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spelling doaj-art-50e34c6ea79545b991cc35ba569296d12025-08-20T03:06:27ZengSpringer NatureMolecular Systems Biology1744-42922016-12-01121211410.15252/msb.20167044Non‐genetic diversity modulates population performanceAdam James Waite0Nicholas W Frankel1Yann S Dufour2Jessica F Johnston3Junjiajia Long4Thierry Emonet5Department of Molecular, Cellular, and Developmental Biology, Yale UniversityDepartment of Molecular, Cellular, and Developmental Biology, Yale UniversityDepartment of Molecular, Cellular, and Developmental Biology, Yale UniversityDepartment of Molecular, Cellular, and Developmental Biology, Yale UniversityDepartment of Physics, Yale UniversityDepartment of Molecular, Cellular, and Developmental Biology, Yale UniversityAbstract Biological functions are typically performed by groups of cells that express predominantly the same genes, yet display a continuum of phenotypes. While it is known how one genotype can generate such non‐genetic diversity, it remains unclear how different phenotypes contribute to the performance of biological function at the population level. We developed a microfluidic device to simultaneously measure the phenotype and chemotactic performance of tens of thousands of individual, freely swimming Escherichia coli as they climbed a gradient of attractant. We discovered that spatial structure spontaneously emerged from initially well‐mixed wild‐type populations due to non‐genetic diversity. By manipulating the expression of key chemotaxis proteins, we established a causal relationship between protein expression, non‐genetic diversity, and performance that was theoretically predicted. This approach generated a complete phenotype‐to‐performance map, in which we found a nonlinear regime. We used this map to demonstrate how changing the shape of a phenotypic distribution can have as large of an effect on collective performance as changing the mean phenotype, suggesting that selection could act on both during the process of adaptation.https://doi.org/10.15252/msb.20167044cellular motilitychemotaxisJensen's inequalitynon‐genetic diversitynonlinear systems
spellingShingle Adam James Waite
Nicholas W Frankel
Yann S Dufour
Jessica F Johnston
Junjiajia Long
Thierry Emonet
Non‐genetic diversity modulates population performance
Molecular Systems Biology
cellular motility
chemotaxis
Jensen's inequality
non‐genetic diversity
nonlinear systems
title Non‐genetic diversity modulates population performance
title_full Non‐genetic diversity modulates population performance
title_fullStr Non‐genetic diversity modulates population performance
title_full_unstemmed Non‐genetic diversity modulates population performance
title_short Non‐genetic diversity modulates population performance
title_sort non genetic diversity modulates population performance
topic cellular motility
chemotaxis
Jensen's inequality
non‐genetic diversity
nonlinear systems
url https://doi.org/10.15252/msb.20167044
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AT junjiajialong nongeneticdiversitymodulatespopulationperformance
AT thierryemonet nongeneticdiversitymodulatespopulationperformance