Folding and cutting DNA into reconfigurable topological nanostructures

Abstract

Topology is the mathematical study of the spatial properties that are preserved through the deformation, twisting and stretching of objects. Topological architectures are common in nature and can be seen, for example, in DNA molecules that condense and relax during cellular events 1 . Synthetic topological nanostructures, such as catenanes and rotaxanes, have been engineered using supramolecular chemistry, but the fabrication of complex and reconfigurable structures remains challenging 2 . Here, we show that DNA origami 3 can be used to assemble a Möbius strip, a topological ribbon-like structure that has only one side [4][5][6] . In addition, we show that the DNA Möbius strip can be reconfigured through strand displacement 7 to create topological objects such as supercoiled ring and catenane structures. This DNA fold-and-cut strategy, analogous to Japanese kirigami 8 , may be used to create and reconfigure programmable topological structures that are unprecedented in molecular engineering.Structural DNA nanotechnology 9 , which makes use of DNA as an information-coding polymer capable of programming nano-structure assembly, has proven its utility in creating sophisticated nanoscale geometrical objects [10][11][12][13][14][15][16] . The recent development of DNA origami 3 , a method that uses short DNA oligos as staples to fold single-stranded genomic DNA scaffolds into geometrically defined two-( ref.3 ) and three-dimensional nanoarchitectures [17][18][19][20][21] , has opened up great opportunities for directed assembly of chemical and biomolecular species with exquisite positional control [22][23][24][25][26] .Engineering topologically complex molecular architectures represents an appealing challenge for chemists and materials scientists, because structures such as catenanes, rotaxanes and knots often display unique material properties 2 . Topological structures have been successfully generated through organic and supramolecular synthesis 27,28 . Earlier works from Seeman and colleagues have exploited enzymatic ligation of simple, branched DNA junctions to create configurations such as various knots 29 and a Borromean ring structure 30 , which were predicated on the relationships between topological crossing points and half-turns within B-DNA or Z-DNA. However, progress using DNA to achieve Here, we demonstrate a DNA origami technique that can be used to create sub-100-nm topological architectures that are reconfigurable. We chose the Möbius strip as our demonstration target, not only because it is artistically inspiring, but also because it will likely display unique material properties 4,5 that may be applied to create novel molecular devices 6 . The Möbius strip has several interesting characteristics. Topologically speaking, it is a surface with only one side and only one boundary. A model can be easily created by taking a paper strip and giving it a half-twist, and then joining the ends of the strip together to form a loop. Cutting along the centre line of the loop destroys a Möbius strip, yieldi...

Programmable motion of DNA origami mechanisms

“…All overhangs on a single link comprised the same sequence so that multiple copies of the same closing strand could actuate the structure. Closing strands contained 5-nt toeholds to allow for their subsequent removal via toehold-mediated strand displacement (30,31) similar to the actuation of the DNA origami Möbius strip (45). TEM images of the DNA origami Bennett linkage are shown in Fig.…”

“…Since then, efforts to fabricate dynamic DNA systems have primarily focused on strand displacement approaches (30) mainly on systems comprising a few strands or arrays of strands undergoing ∼nm-scale motions (31-37) in some cases guided by DNA origami templates (38)(39)(40). More recently, strand displacement has been used to reconfigure DNA origami nanostructures, for example opening DNA containers (19,41,42), controlling molecular binding (43,44), or reconfiguring structures (45). The largest triggerable structural change was achieved by Han et al in a DNA origami Möbius strip (one-sided ribbon structure) that could be opened to approximately double in size (45).…”

“…More recently, strand displacement has been used to reconfigure DNA origami nanostructures, for example opening DNA containers (19,41,42), controlling molecular binding (43,44), or reconfiguring structures (45). The largest triggerable structural change was achieved by Han et al in a DNA origami Möbius strip (one-sided ribbon structure) that could be opened to approximately double in size (45). Constrained motion has been achieved in systems with rotational motion (19,20,32,41,44,46,47) in some cases to open lid-like components (19,20,41) or detect molecular binding (44,48,49).…”

Topological zoo of free-standing knots in confined chiral nematic fluids

“…Knotting and linking are not limited to ropes 4 and are observed even at a molecular level in DNA 5,6 , polymers 7,8 and single molecules 9 . However, the intricacy of knots in physical systems extends beyond basic mathematical notions of knot theory if the knot is a part of a continuum field.…”

Returning to the fold

“…Controlled curvature was achieved in both two and three dimensions to generate shapes such as concentric rings, spheres and ellipsoids 7 . In another variation, 'DNA kirigami' -the folding and cutting of DNA into reconfigurable topological nanostructureswas applied for the synthesis of a Möbius strip and catenated twisted cylinders 8 . In terms of geometry, there were seemingly few limitations to what could be achieved with DNA origami.…”