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

Author(s): Nikolic, Nela; Schreiber, Frank; Dal Co, Alma; Kiviet, Daniel J; Bergmiller, Tobias; Littmann, Sten; Kuypers, Marcel M; Ackermann, Martin
Article Title: Cell-to-cell variation and specialization in sugar metabolism in clonal bacterial populations
Affiliation IST Austria
Abstract: 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.
Journal Title: PLoS Genetics
Volume: 13
Issue 12
ISSN: 1553-7404
Publisher: Public Library of Science  
Date Published: 2017-12-18
Start Page: Articel number: e1007122
Copyright Statement: CC BY
DOI: 10.1371/journal.pgen.1007122
Notes: We are grateful to Alex Böhm (1971–2012), Markus Arnoldini, Manuel Hörl, Nikki Freed, Dominik Refardt, and Olin Silander for useful discussions and technical advice. Also, we thank Markus Arnoldini, Daniela Tienken, Aurelia Kollros, and Thomas Barner for their assistance with the experiments. We acknowledge technical assistance of The Flow Cytometry Core Facility of ETH Zurich as well as Joachim Hehl and the Scientific Center for Optical and Electron Microscopy (ScopeM) of ETH Zurich. NN is grateful to Călin C. Guet for his support. NN and TB were supported by the Swiss National Science Foundation grant 31003A_130735 to MA. NN was supported by the FEMS Research Grant for visits to the MPI for Marine Microbiology in Bremen, Germany. NN is currently supported by the ISTFELLOW program of the IST Austria and the European Commission. FS was supported by a Leopoldina postdoctoral fellowship (LPDS 2009-42), a Marie-Curie-Intra-European fellowship for career development (FP7-MC-IEF; 271929; Phenofix), a Synthesis Grant of the ETH Zurich Center for Adaptation to a Changing Environment (ACE), and by Eawag. DJK was supported by the ETH Fellowship program. ADC and DJK were supported by the Swiss National Science Foundation grant 31003A_149267 to MA. SL and MMMK were supported by the Max Planck Society. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Open access: yes (OA journal)