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...

Full description

Bibliographic Details
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
_version_ 1797280641003290624
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
work_keys_str_mv AT adamjameswaite nongeneticdiversitymodulatespopulationperformance
AT nicholaswfrankel nongeneticdiversitymodulatespopulationperformance
AT yannsdufour nongeneticdiversitymodulatespopulationperformance
AT jessicafjohnston nongeneticdiversitymodulatespopulationperformance
AT junjiajialong nongeneticdiversitymodulatespopulationperformance
AT thierryemonet nongeneticdiversitymodulatespopulationperformance