Sugar Influx Sensing by the Phosphotransferase System of Escherichia coli

PLoS Biol. 2016 Aug 24;14(8):e2000074. doi: 10.1371/journal.pbio.2000074. eCollection 2016 Aug.

Abstract

The phosphotransferase system (PTS) plays a pivotal role in the uptake of multiple sugars in Escherichia coli and many other bacteria. In the cell, individual sugar-specific PTS branches are interconnected through a series of phosphotransfer reactions, thus creating a global network that not only phosphorylates incoming sugars but also regulates a number of cellular processes. Despite the apparent importance of the PTS network in bacterial physiology, the holistic function of the network in the cell remains unclear. Here we used Förster resonance energy transfer (FRET) to investigate the PTS network in E. coli, including the dynamics of protein interactions and the processing of different stimuli and their transmission to the chemotaxis pathway. Our results demonstrate that despite the seeming complexity of the cellular PTS network, its core part operates in a strikingly simple way, sensing the overall influx of PTS sugars irrespective of the sugar identity and distributing this information equally through all studied branches of the network. Moreover, it also integrates several other specific metabolic inputs. The integrated output of the PTS network is then transmitted linearly to the chemotaxis pathway, in stark contrast to the amplification of conventional chemotactic stimuli. Finally, we observe that default uptake through the uninduced PTS network correlates well with the quality of the carbon source, apparently representing an optimal regulatory strategy.

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Biological Transport
  • Calcium-Binding Proteins / genetics
  • Calcium-Binding Proteins / metabolism
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Escherichia coli / genetics
  • Escherichia coli / metabolism*
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism*
  • Fluorescence Resonance Energy Transfer / methods
  • Hexoses / metabolism*
  • Hexoses / pharmacokinetics
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Monosaccharide Transport Proteins / genetics
  • Monosaccharide Transport Proteins / metabolism
  • Periplasmic Binding Proteins / genetics
  • Periplasmic Binding Proteins / metabolism
  • Phosphate-Binding Proteins
  • Phosphoenolpyruvate Sugar Phosphotransferase System / genetics
  • Phosphoenolpyruvate Sugar Phosphotransferase System / metabolism*
  • Phosphorylation
  • Protein Binding
  • Signal Transduction

Substances

  • Bacterial Proteins
  • Calcium-Binding Proteins
  • Carrier Proteins
  • Escherichia coli Proteins
  • Hexoses
  • Luminescent Proteins
  • Monosaccharide Transport Proteins
  • NPr protein, E coli
  • Periplasmic Binding Proteins
  • Phosphate-Binding Proteins
  • crr protein, E coli
  • galactose-binding protein
  • Phosphoenolpyruvate Sugar Phosphotransferase System
  • phosphocarrier protein HPr

Grant support

Deutsche Forschungsgemeinschaft www.dfg.de (grant number SO 421/7-2).Received by VS and RS. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. European Research Council www.erc.europa.eu (grant number 294761-MicRobE).Received by VS and BG. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.