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...
Main Authors: | , , , , , |
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Format: | Article |
Language: | English |
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Springer Nature
2016-12-01
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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. |
first_indexed | 2024-03-07T16:44:12Z |
format | Article |
id | doaj.art-50e34c6ea79545b991cc35ba569296d1 |
institution | Directory Open Access Journal |
issn | 1744-4292 |
language | English |
last_indexed | 2024-03-07T16:44:12Z |
publishDate | 2016-12-01 |
publisher | Springer Nature |
record_format | Article |
series | Molecular Systems Biology |
spelling | doaj.art-50e34c6ea79545b991cc35ba569296d12024-03-03T07:05:21ZengSpringer NatureMolecular Systems Biology1744-42922016-12-011212n/an/a10.15252/msb.20167044Non‐genetic diversity modulates population performanceAdam James Waite0Nicholas W Frankel1Yann S Dufour2Jessica F Johnston3Junjiajia Long4Thierry Emonet5Department of Molecular, Cellular, and Developmental Biology Yale University New Haven CT USADepartment of Molecular, Cellular, and Developmental Biology Yale University New Haven CT USADepartment of Molecular, Cellular, and Developmental Biology Yale University New Haven CT USADepartment of Molecular, Cellular, and Developmental Biology Yale University New Haven CT USADepartment of Physics Yale University New Haven CT USADepartment of Molecular, Cellular, and Developmental Biology Yale University New Haven CT USAAbstract 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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