Pathway Complexity in Fuel-Driven DNA Nanostructures with Autonomous Reconfiguration of Multiple Dynamic Steady States

We introduce pathway complexity on a multicomponent systems level in chemically fueled transient DNA polymerization system. The systems are based on a monomeric species pool that is fueled by ATP and orchestrated by an enzymatic reaction network (ERN) of ATP-powered ligation and concurrent cleavage. Such systems display autonomous evolution over multiple structural dynamic steady states from monomers to dimers, oligomer of dimers to ultimately randomized polymer structure before being ultimately degraded back to monomers once the fuel is consumed. The enabling key principle is to design monomer species having kinetically selected molecular recognition with respect to the structure-forming step (ATP-powered ligation) by encoding different sticky-end overhangs into the ligation area. However, all formed structures are equally degraded, and the orthogonal molecular recognition of the different starting species are harmonized during the constantly occurring restriction process, leading in consequence to a reconfiguration of the driven dynamic nanostructures on a higher hierarchical level. This non-equilibrium systems chemistry approach to pathway complexity provides new conceptual insights in fuel-driven automatons and autonomous materials design.