Colloquium Natural and Life Sciences - Andreas Walther

 ATP‐driven Non‐Equilibrium Systems

Active biological materials perform under non-equilibrium conditions by a constant exchange of energy and matter, which makes them functional and adaptive to environmental changes.[1,2] Microtubules are the prime example of dissipative structure formation in the cell. Those cytoskeletal filaments polymerize dynamically in response to the cellular needs driven by the hydrolysis of guanosine triphosphate (GTP).

Inspired by the dynamics and adaptivity of microtubules, we developed an ATP-fueled dynamic-covalent polymerization system of DNA chains with programmable transient steady states. Short synthetic DNA monomer strands are embedded into a competing enzymatic reaction network of an ATP-dependent DNA ligase and a counteracting endonuclease. Antagonistic action of both enzymes creates a universal dynamic covalent phosphodiester bond, whose overall average bond strength is coupled to the energy dissipation kinetics under biocatalytic control and translates directly into the dynamic steady state (DySS) properties of the DNA polymers.

We show how to program the lifetime, the average degree of polymerization and intermolecular exchange frequencies of the DySS polymers in dependence of the ATP fuel and the enzyme concentrations. Critically, the system can be refueled and adapts autonomously to changes in its environment. Integration of this fuel-driven dynamic covalent bond into self-sorting colloidal systems or systems undergoing liquid/liquid phase separation are discussed.