An Optimal Free Energy Dissipation Strategy of the MinCDE Oscillator in Regulating Symmetric Bacterial Cell Division

PLoS Comput Biol. 2015 Aug 28;11(8):e1004351. doi: 10.1371/journal.pcbi.1004351. eCollection 2015 Aug.

Abstract

Sustained molecular oscillations are ubiquitous in biology. The obtained oscillatory patterns provide vital functions as timekeepers, pacemakers and spacemarkers. Models based on control theory have been introduced to explain how specific oscillatory behaviors stem from protein interaction feedbacks, whereas the energy dissipation through the oscillating processes and its role in the regulatory function remain unexplored. Here we developed a general framework to assess an oscillator's regulation performance at different dissipation levels. Using the Escherichia coli MinCDE oscillator as a model system, we showed that a sufficient amount of energy dissipation is needed to switch on the oscillation, which is tightly coupled to the system's regulatory performance. Once the dissipation level is beyond this threshold, unlike stationary regulators' monotonic performance-to-cost relation, excess dissipation at certain steps in the oscillating process damages the oscillator's regulatory performance. We further discovered that the chemical free energy from ATP hydrolysis has to be strategically assigned to the MinE-aided MinD release and the MinD immobilization steps for optimal performance, and a higher energy budget improves the robustness of the oscillator. These results unfold a novel mode by which living systems trade energy for regulatory function.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Cell Cycle Proteins / metabolism*
  • Cell Division / physiology*
  • Computational Biology
  • Computer Simulation
  • Escherichia coli / physiology
  • Escherichia coli Proteins / metabolism*
  • Models, Biological*
  • Thermodynamics

Substances

  • Cell Cycle Proteins
  • Escherichia coli Proteins
  • Adenosine Triphosphate

Grants and funding

LX and GL are partially supported by the Columbian College Facilitating Fund from the George Washington University and the Outreach Pilot Award from Johns Hopkins University (2001907751 to GL). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.