Spontaneous Reorganization of DNA-Based Polymers in Higher Ordered Structures Fueled by RNA.

Serena Gentile,Leonard J Prins,Passa E Pungchai,Erica Del Grosso,Francesco Ricci,Elisa Franco

doi:10.1021/jacs.1c09503

Abstract

We demonstrate a strategy that allows for the spontaneous reconfiguration of self-assembled DNA polymers exploiting RNA as chemical fuel. To do this, we have rationally designed orthogonally addressable DNA building blocks that can be transiently deactivated by RNA fuels and subtracted temporarily from participation in the self-assembly process. Through a fine modulation of the rate at which the building blocks are reactivated we can carefully control the final composition of the polymer and convert a disordered polymer in a higher order polymer, which is disfavored from a thermodynamic point of view. We measure the dynamic reconfiguration via fluorescent signals and confocal microscopy, and we derive a kinetic model that captures the experimental results. Our approach suggests a novel route toward the development of biomolecular materials in which engineered chemical reactions support the autonomous spatial reorganization of multiple components.

Highlights

Life is a nonequilibrium state of matter that is maintained at the expense of energy.[1]
Whereas traditionally the focus has been on the assembly product with the highest thermodynamic stability,[18] recently it has been shown that different kinetic products can be selectively obtained from the same building blocks by carefully designing the supramolecular kinetic pathways leading to their formation.[19,20]
The combined use of both tiles for selfassembly can lead to different polymers depending on the organization of the tiles: homopolymers are structures that consist of one type of tile, block copolymers contain segments of tiles of the same type, and in random copolymers the two tiles are randomly distributed

Summary

■ INTRODUCTION

Life is a nonequilibrium state of matter that is maintained at the expense of energy.[1]. We and others have recently shown that DNA offers tremendous opportunities in the field of chemically fueled selfassembly[23−28] because (1) hybridization and strand exchange reactions are highly predictable from both a thermodynamic and kinetic point of view, (2) a myriad of enzymes are available to regulate nucleic acid fuel-to-waste conversion with high efficiency and selectivity, and (3) the multivalent nature of DNA hybridization generates a high tolerance to waste accumulation These properties have been used to establish methods to transiently assemble and disassemble polymeric DNA structures, for example, as a result of enzymatic RNA production to activate components and promote their assembly and RNA degradation to cause the assemblies to collapse.[25−27,39] spontaneous DNA polymer assembly and disassembly can be achieved by using DNA nicking and ligation reactions.[29]. Our strategy allows us to shuttle the system in a controlled fashion between different kinetic states just by adding the appropriate RNA fuel and it permits the population of an energetically uphill state, which is entropically disfavored

■ RESULTS AND DISCUSSION

■ CONCLUSION

■ ACKNOWLEDGMENTS

■ REFERENCES