More ATP Does Not Equal More Contractility: Power And Remodelling In Reconstituted Actomyosin

TL;DR

This study reveals that higher ATP levels lead to less contractility and different pattern formations in actomyosin networks, explained by a new active hydrodynamic theory linking ATP concentration to myosin minifilament behavior.

Contribution

The paper introduces a polar active hydrodynamic model that connects ATP concentration to actomyosin pattern formation and contractility, supported by microscopic stochastic descriptions.

Findings

High ATP induces swirling patterns in actomyosin networks.

Low ATP results in aster-like structures.

ATP reduces contractile force generation by myosin minifilaments.

Abstract

The cytoskeletal component actomyosin is a canonical example of active matter since the powerstroke cycle locally converts chemical energy in the form of adenoside triphosphate (ATP) into mechanical work for remodelling. Observing myosin II minifilaments as they remodel actin {\it in vitro}, we now report that: at high concentrations of ATP, myosin minifilaments form metastable swirling patterns that are characterised by recurrent vortex and spiral-like motifs, whereas; at low concentrations of ATP, such structures give way to aster-like patterns. To explain this, we construct the (quasi-)steady states of a polar active hydrodynamic theory of actomyosin whose ATP-scaling is obtained from a microscopic, stochastic description for the ATP-dependent binding of the heads of single myosin II minifilaments. The latter codifies the heuristic that, since the powerstroke cycle involves the unbinding of myosin II heads from actin, increases in the concentration of ATP reduce the likelihood that a given myosin II minifilament has more than one head bound simultaneously, reducing its ability to generate contractile forces and increasing the relative likelihood of processive motion. This reproduces several qualitative and some quantitative aspects of experiments, providing evidence for the central phenomenon of the theory: an ATP-dependent active contractile instability. ATP therefore controls not only the rate at which work is done -- \textit{i.e.,} the power -- but also the mode by which this occurs.