Cell-to-cell variation and specialization in sugar metabolism in clonal bacterial populations.

While we have good understanding of bacterial metabolism at the population level, we know little about the metabolic behavior of individual cells: do single cells in clonal populations sometimes specialize on different metabolic pathways? Such metabolic specialization could be driven by stochastic g...

Full description

Bibliographic Details
Main Authors: Nela Nikolic, Frank Schreiber, Alma Dal Co, Daniel J Kiviet, Tobias Bergmiller, Sten Littmann, Marcel M M Kuypers, Martin Ackermann
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-12-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC5773225?pdf=render
_version_ 1819150394268319744
author Nela Nikolic
Frank Schreiber
Alma Dal Co
Daniel J Kiviet
Tobias Bergmiller
Sten Littmann
Marcel M M Kuypers
Martin Ackermann
author_facet Nela Nikolic
Frank Schreiber
Alma Dal Co
Daniel J Kiviet
Tobias Bergmiller
Sten Littmann
Marcel M M Kuypers
Martin Ackermann
author_sort Nela Nikolic
collection DOAJ
description While we have good understanding of bacterial metabolism at the population level, we know little about the metabolic behavior of individual cells: do single cells in clonal populations sometimes specialize on different metabolic pathways? Such metabolic specialization could be driven by stochastic gene expression and could provide individual cells with growth benefits of specialization. We measured the degree of phenotypic specialization in two parallel metabolic pathways, the assimilation of glucose and arabinose. We grew Escherichia coli in chemostats, and used isotope-labeled sugars in combination with nanometer-scale secondary ion mass spectrometry and mathematical modeling to quantify sugar assimilation at the single-cell level. We found large variation in metabolic activities between single cells, both in absolute assimilation and in the degree to which individual cells specialize in the assimilation of different sugars. Analysis of transcriptional reporters indicated that this variation was at least partially based on cell-to-cell variation in gene expression. Metabolic differences between cells in clonal populations could potentially reduce metabolic incompatibilities between different pathways, and increase the rate at which parallel reactions can be performed.
first_indexed 2024-12-22T14:16:48Z
format Article
id doaj.art-e3bf80cf6fab46c7977f843347ab8d04
institution Directory Open Access Journal
issn 1553-7390
1553-7404
language English
last_indexed 2024-12-22T14:16:48Z
publishDate 2017-12-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Genetics
spelling doaj.art-e3bf80cf6fab46c7977f843347ab8d042022-12-21T18:23:06ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042017-12-011312e100712210.1371/journal.pgen.1007122Cell-to-cell variation and specialization in sugar metabolism in clonal bacterial populations.Nela NikolicFrank SchreiberAlma Dal CoDaniel J KivietTobias BergmillerSten LittmannMarcel M M KuypersMartin AckermannWhile we have good understanding of bacterial metabolism at the population level, we know little about the metabolic behavior of individual cells: do single cells in clonal populations sometimes specialize on different metabolic pathways? Such metabolic specialization could be driven by stochastic gene expression and could provide individual cells with growth benefits of specialization. We measured the degree of phenotypic specialization in two parallel metabolic pathways, the assimilation of glucose and arabinose. We grew Escherichia coli in chemostats, and used isotope-labeled sugars in combination with nanometer-scale secondary ion mass spectrometry and mathematical modeling to quantify sugar assimilation at the single-cell level. We found large variation in metabolic activities between single cells, both in absolute assimilation and in the degree to which individual cells specialize in the assimilation of different sugars. Analysis of transcriptional reporters indicated that this variation was at least partially based on cell-to-cell variation in gene expression. Metabolic differences between cells in clonal populations could potentially reduce metabolic incompatibilities between different pathways, and increase the rate at which parallel reactions can be performed.http://europepmc.org/articles/PMC5773225?pdf=render
spellingShingle Nela Nikolic
Frank Schreiber
Alma Dal Co
Daniel J Kiviet
Tobias Bergmiller
Sten Littmann
Marcel M M Kuypers
Martin Ackermann
Cell-to-cell variation and specialization in sugar metabolism in clonal bacterial populations.
PLoS Genetics
title Cell-to-cell variation and specialization in sugar metabolism in clonal bacterial populations.
title_full Cell-to-cell variation and specialization in sugar metabolism in clonal bacterial populations.
title_fullStr Cell-to-cell variation and specialization in sugar metabolism in clonal bacterial populations.
title_full_unstemmed Cell-to-cell variation and specialization in sugar metabolism in clonal bacterial populations.
title_short Cell-to-cell variation and specialization in sugar metabolism in clonal bacterial populations.
title_sort cell to cell variation and specialization in sugar metabolism in clonal bacterial populations
url http://europepmc.org/articles/PMC5773225?pdf=render
work_keys_str_mv AT nelanikolic celltocellvariationandspecializationinsugarmetabolisminclonalbacterialpopulations
AT frankschreiber celltocellvariationandspecializationinsugarmetabolisminclonalbacterialpopulations
AT almadalco celltocellvariationandspecializationinsugarmetabolisminclonalbacterialpopulations
AT danieljkiviet celltocellvariationandspecializationinsugarmetabolisminclonalbacterialpopulations
AT tobiasbergmiller celltocellvariationandspecializationinsugarmetabolisminclonalbacterialpopulations
AT stenlittmann celltocellvariationandspecializationinsugarmetabolisminclonalbacterialpopulations
AT marcelmmkuypers celltocellvariationandspecializationinsugarmetabolisminclonalbacterialpopulations
AT martinackermann celltocellvariationandspecializationinsugarmetabolisminclonalbacterialpopulations