Chemophoresis engine: A general mechanism of ATPase-driven cargo transport

PLoS Comput Biol. 2022 Jul 25;18(7):e1010324. doi: 10.1371/journal.pcbi.1010324. eCollection 2022 Jul.

Abstract

Cell polarity regulates the orientation of the cytoskeleton members that directs intracellular transport for cargo-like organelles, using chemical gradients sustained by ATP or GTP hydrolysis. However, how cargo transports are directly mediated by chemical gradients remains unknown. We previously proposed a physical mechanism that enables directed movement of cargos, referred to as chemophoresis. According to the mechanism, a cargo with reaction sites is subjected to a chemophoresis force in the direction of the increased concentration. Based on this, we introduce an extended model, the chemophoresis engine, as a general mechanism of cargo motion, which transforms chemical free energy into directed motion through the catalytic ATP hydrolysis. We applied the engine to plasmid motion in a ParABS system to demonstrate the self-organization system for directed plasmid movement and pattern dynamics of ParA-ATP concentration, thereby explaining plasmid equi-positioning and pole-to-pole oscillation observed in bacterial cells and in vitro experiments. We mathematically show the existence and stability of the plasmid-surfing pattern, which allows the cargo-directed motion through the symmetry-breaking transition of the ParA-ATP spatiotemporal pattern. We also quantitatively demonstrate that the chemophoresis engine can work even under in vivo conditions. Finally, we discuss the chemophoresis engine as one of the general mechanisms of hydrolysis-driven intracellular transport.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphatases* / metabolism
  • Adenosine Triphosphate / metabolism
  • Biological Transport
  • Organelles* / metabolism
  • Plasmids

Substances

  • Adenosine Triphosphate
  • Adenosine Triphosphatases

Grants and funding

This work was supported by Japan Society for the Promotion of Science (JSPS) KAKENHI Grant No. 19H05796,17H06386, 17K15050 and Novo Nordisk Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.