Abstract
The seminal recognition by Ned Seeman that DNA could be programmed via base-pairing to form higher order structures is well known. What may have been partially forgotten is one of Dr. Seeman’s strong motivations for forming precise and programmable nanostructures was to create nanoelectronic devices. This motivation is particularly apt given that modern electronic devices require precision positioning of conductive elements to modulate and control electronic properties, and that such positioning is inherently limited by the scaling of photoresist technologies: DNA may literally be one of the few ways to make devices smaller (Liddle and Gallatin in Nanoscale 3:2679–2688 [1]). As with many other insights regarding DNA at the nanoscale, Ned Seeman recognized the possibilities of DNA-templated electronic devices as early as 1987 (Robinson and Seeman in Protein Eng. 1:295–300 [2]). As of 2002, Braun’s group attempted to develop methods for lithography that involved metalating DNA (Keren et al. in Science 297:72–75 [3]). However, this instance involved linear, double-stranded DNA, in which portions were separated using RecA, and thus, the overall complexity of the lithography was limited. Since then, the extraordinary control afforded by DNA nanotechnology has provided equally interesting opportunities for creating complex electronic circuitry, either via turning DNA into an electronic device itself (Gates et al. in Crit. Rev. Anal. Chem. 44:354–370 [4]), or by having DNA organize other materials (Hu and Niemeyer in Adv. Mat. 31(26), [5]) that can be electronic devices (Dai et al. in Nano Lett. 20:5604–5615 [6]).
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1 Origami’s Rise
While Ned Seeman can be almost uniquely attributed with the idea that DNA could be designed to assemble into higher order supramolecular structures [7], the means by which these structures would be created has varied over the years [8, 9]. Early efforts to generate non-extensible structures (such as the Olympian Borromean rings [10]) were followed by the creation of rigid, modular DNA elements based on more rigid crossover structures resembling Holliday junctions (the so-called double crossover or DX tile; Fig. 1a [11]) that could be assembled as building blocks into larger architectures [12] (Fig. 1b). Attempts to precisely control architecture from the atomic level upwards were further encouraged by Rothemund’s discovery that short oligonucleotide “staples” could be used to fold longer DNAs into defined “origami” shapes [13] (Fig. 1c). This realization has since exploded into a huge range of architectures, both two- and three-dimensional [14], marvelous artistic endeavors [15], and a range of potential application areas for origami [16]. Further extending the departure from atomic level control, there is even tantalizing evidence that extensible three-dimensional crystal structures can arise, albeit somewhat fortuitously, allowing enhanced engineering of DNA lattice dimensions [17]. These progressive advances in atomic scale control over complex structure now provide intriguing opportunities for configuring electronics.
2 Making DNA Nanostructures Conductive Through Metallization
In order to make DNA nanostructures into electronic devices, one approach is to determine how to make DNA conductive. While there is some evidence that DNA itself can be a conductive material [19, 20], its conductivity is relatively low [21]. To solve this problem, nucleic acids can interact with metals (or be modified to interact with metals), and if completely metalated can readily pass current. To this end, Yan et al. constructed nanogrid and nanoribbon lattices from four arm junctions and used a two-step procedure involving aldehyde derivatization of the DNA, silver seeding, and then complete silver metalation to create conductive nanowires [22] (Fig. 2a). The metallized nanowires showed a linear-ohmic current–voltage (I-V) profile using a two-terminal setup. The bulk resistivities of the nanoribbon structures were 2.4 × 10–6 Ω·m, roughly 100-fold more than polycrystalline silver (1.6 × 10–8 Ω·m). The higher resistance could be due to the difficulty in calculating the true unit cross-section of the silver, granularity in the silver structure, or low densities of the metals following deposition. Nonetheless, this was one of the first demonstrations that organized DNA assemblies might eventually prove useful for the creation of programmable electronic devices. Following up this feat, the LaBean lab then created and metalated nanotubes (Fig. 2b) [23] based on triple-crossover tiles (TX, previously developed in collaboration with the Seeman lab [24]). These structures were found to have around a tenfold higher resistance compared to the nanoribbon strategy, however, still showed the ohmic behavior of silver expected of a conductive metal structure.
In an exciting recent result, Shani et al. became the first to report superconducting nanowires based on metalated DNA [25]. Niobium nitride, a material known to become a superconductor below 16 K, was deposited onto the surface of DNA using magnetron sputtering (Fig. 2c). The coated DNA exhibited a superconducting transition at approximately 5 K, ascribed to thermally activated phase slips, with further improvements in conductivity with the onset of quantum phase slips at 3.7 K. The DNA-templated superconductor exhibited maximal conductivity at the lowest measured temperature of 2.2 K and also showed a large negative magnetoresistance, further indicative of superconducting properties.
Conductivity alone is only one aspect of an electronic device, and thus, there is a continuing need to direct particular electron flows. The irregular nature of DNA origami provides opportunities for creating virtually any pattern, and the Harb and Wooley labs in turn metalated [26] and demonstrated the conductivity [27] of origami, including plating branched structures (Fig. 2d). Of course, mere patterning is not necessarily sufficient to create functional electronic junctions. Strategies for diversifying electronic interfaces include hybridization of DNA-conjugated gold nanoparticles to allow site-specific seeding [28] and organic masking to deposit different metals [29]. Another approach has been to sacrifice continuity of charge transport in favor of creating specific metalated structures side-by-side on “nanoscale printed circuit boards” [30]. The characterization of conductance on C-shaped origami nanowires has indicated a variety of modes of charge transport, including hopping, thermionic, and tunneling mechanisms [31].
Despite the wealth of shapes and patterns afforded by DNA, a variety of methods for casting and plating, numerous possible charge transport mechanisms, and nanoscale electronic devices have for the most part not yet emerged from attempts to generating conductive DNA. This is in part because of the difficulties in actually forming the equivalent of atomic scale bandgap p-n junctions that are key to all electronics (and hauntingly were also key to Seeman's original dreams for self-assembled memories devices [2]).
While these difficulties may yet be overcome via even more refined and specific methods for metal placement and coating on DNA, an alternative approach has arisen in which the key advantage of nanoscale placement, rather than nanoscale patterning, is emphasized.
3 Decorating Origami
Moore’s law is of course an observation, rather than a requirement, and suggests that the number of transistors within an integrated circuit will double approximately every two years. As we reach the limitations of lithography methods to achieve ever-increasing circuit densities for advanced computation, alternative fabrication techniques are being explored. In particular, DNA nanotechnology has the theoretical ability to pattern semiconducting elements with sub-nm resolution (since the width of ssDNA is ca. 0.9 nm) and could potentially be used in moderate throughput for the bottom-up, self-assembled fabrication of semiconducting chips.
3.1 DNA Scaffolding for Conductive Metals
While it has proven possible to make origami itself conductive, origami can also be used as an armature or scaffold for identifying, sorting, and positioning conductive elements. This has been achieved with a variety of DNA-material hybrids, including gold nanoparticles [33, 34], nanorods [35, 36], and quantum dots [37]. These hybrids can be further organized into higher order conductive structures. For example, Chad Mirkin’s group created spherical nucleic acids (SNA) [33], and three-dimensional nucleic acid nanostructures composed of a nanoparticle core (commonly gold) densely functionalized with DNA. By functionalizing SNAs with DNA sequences that could recognize planar nanoparticle clusters, Oleg Gangs’ group created electronically conductive stacked supramolecular assemblies [38] (Fig. 3a). These assemblies were capable of forming filament-like, pillar structures, comprised of alternating SNAs and planar nanoparticles. By controlling the number, position, size, and composition of the nanoparticles, different three-dimensional pillar architectures could be produced with a variety of physical and electrical transport properties.
DNA origami has also been used as a scaffold to assemble single metal wires composed of contiguous electrically connected metal–semiconductor junctions. In 2020, Aryal et al. [39] deposited DNA origami onto a silicon wafer then positioned three DNA-coated gold nanorods (100 nm × 20 nm) along the DNA with increasing gaps between the nanorods (Fig. 3b). Next, tellurium nanorods were positioned into the gaps between the gold nanorods via electrostatic interactions. Finally, the gaps between the nanorods were filled via electroless gold plating, creating a nanoscale wire composed of alternating Au-Te-Au junctions. When subjected to current–voltage (I-V) electrical characterization, the response showed a non-linear-ohmic nature consistent with Schottky junction (aka Schottky barrier diode) properties. This was the first demonstration of how DNA origami can be used to assemble nanoscale metal–semiconductor junctions.
3.2 DNA Scaffolds for Conductive Polymers
An alternative to introducing metals into DNA origami materials is the incorporation of conductive polymers into the origami. This was originally accomplished by the Gothelf and Dong labs; a conjugated paraphenylene vinylene (APPV) brush polymer that contained a nine nucleotide single-stranded DNA staple was synthesized [40]. To program the placement of the APPV onto a silicon oxide substrate and resultant architectures, DNA origami that could hybridize to the oligonucleotide attached to the polymer was constructed. Using this method, the authors were able to direct the placement and orientation of the APPV-DNA hybrid to create linear structures, 90° curves, U-shape, staircases, and circular designs (Fig. 3c). Ultimately, three-dimensional cylindrical DNA origami structures were constructed, and APPV was routed around. While in this implementation, no electrical conductivity measurements were performed, but the surface potential of the APPV-DNA polymer chain was measured to be -130 mV, implying a charge transfer higher than the underlying silicon oxide. These results provide an excellent proof-of-principle for extension to more conductive polymers and demonstrate the ability to create very compact three-dimensional structures capable of organizing conductive polymers into molecular-scale electronics, with the polymer providing a link to softer, flexible, and perhaps more biocompatible materials for biomedical engineering applications.
3.3 DNA Scaffolds for Carbon Nanotubes
The DNA-based placement of conductive and now semi-conductive metals is powerful, but electronic applications remain elusive because of a need for scaling, an application that may yet arise via the placement of carbon nanotubes (CNTs); though in particular, controlling the placement and positioning of CNTs in three-dimensions is incredibly complicated. Structural precision can potentially be achieved without DNA using thin-film approaches, but these are prone to assembly defects such as crossing, bundling, and non-conforming pitch [41], parameters essential for creating a precisely ordered three-dimensional CNT architecture for applications in integrated circuits. Utilization of DNA nanostructures as templates will allow greater precision in the nanofabrication process. If architectural problems are overcome, CNT-based computers can potentially outperform the best silicon devices [42], while being at least an order of magnitude more efficient [43]. This efficiency is incredibly important in regard to Dennard Scaling, which states that as a transistor reduces in size, the power density stays constant. This reduction in power usage allows manufacturers to increase the operating frequency of microprocessors and boost performance. Over the past 5 years, there has not been a significant increase in operating frequency, with IC manufacturers resorting to multi-core threading to overcome performance restrictions. Using new highly efficient materials such as CNTs would enable manufacturers to go beyond silicon-based ICs and increase operating frequency with less impact on power requirements.
In 2003, Zheng et al. [44] reported that ssDNA can strongly interact with CNTs to form a stable complex; this advance most importantly allowed CNTs to be solubilized in aqueous solutions. The DNA-CNT hybrid architecture (wrapping) was found to be dependent on a short (10–45 nucleotide) GT-rich sequence which could form a two-dimensional sheet structure. Furthermore, it has been discovered that the chirality of the DNA around the CNT is dependent on the handedness of the helicity of the DNA [45]. Remarkably, GT-rich elements can selectively bind all 12 of the major chiral semiconducting CNT species [46]. The wrapping of the negatively charged DNA around the CNTs was also found to promote the selective separation of chirally pure CNTs via a positively charged anion exchange resin [46], potentially solving one of the major application challenges for CNTs, since chiral structures cannot be readily synthesized but have superior electrical conductivity and semiconducting properties [47].
These results set the stage for using DNA origami to fabricate highly specific and orientated nanostructures with CNTs. An inherent problem with using CNTs is the difficulty of organizing them into specific orientations. This complication was nicely remedied by Erik Winfrees’ group, who used DNA origami with “hook-binding domains” to perpendicularly place two CNTs into a specific two-dimensional orientation [48] (Fig. 4a). The alignment of the CNTs into cross-junctions positioned them with 6 nm resolution and led to a stable field-effect transistor (FET)-like behavior, two firsts. This was quickly followed by the Goddard group using small-structured DNA linkers to establish highly dense parallel CNT arrays that could be self-assembled on the surface of mica (Fig. 4b). By tuning the length of the DNA linker, the CNT pitch could be tuned accordingly, with distances ranging from <3 nm to >20 nm [49]. Using a different DNA origami architecture that resulted in parallel placements, the Norton group utilized larger “blocks” of DNA origami that acted as linkers to orient two CNTs onto a one-dimensional origami construct, separating CNTs of ~100 nm length by more than 500 nm (Fig. 4c) [50]. Alternative methods of assembling CNTs on DNA origami templates using streptavidin–biotin interactions have also proven successful in generating defined cross-junctions [51].
Even more complex “Y-shape” nanostructures have been created that involve a three-way DNA junction with protruding single-stranded sequences that anneal to CNTs. These nanostructures orient the three CNTs at an approximate 120° angle to each other. Further, higher-ordered networks of each Y-shaped triplet can be assembled to create a DNA-CNT “mesh” [52]. Recently, Seeman’s group [53] has demonstrated that rather than absorbing DNA to the sides of SWCNTs via van der Waals forces, DNA can be specifically localized to the ends of SWCNT structures via conjugation chemistry between a pendant amino-group on the DNA molecule and carboxylates presented on the termini of the SWCNT. By orienting DNA to the terminals of the nanotubes, the conductive lattice structure on the sides is not impeded, reducing interference with the electrical properties of the SWCNT. The ssDNA conjugated to the reactive end of a SWCNT can thus be used to orient multiple nanotubes via hybridization, creating precisely positioned SWCNTs within a two-dimensional DNA origami “raft” [53] (Fig. 4d). In another approach to organizing supramolecular structures, a conductive SNA nanoparticle “linker” was used for the parallel positioning of DNA-conjugated carbon nanotubes, resulting in a five-fold binding improvement over just relying on the stickiness of the nanotubes themselves [54].
3.4 Highly Ordered, Three-Dimensional DNA-CNT Arrays
Two publications, released on the same day, go a long way toward the implementation of direct biotemplated CNT nanofabrication using DNA origami “bricks.” Sun et al., [55], developed a highly scalable supramolecular assembly method, termed Spatially Hindered Integration of Nanotube Electronics (SHINE). Densely parallel, aligned arrays of CNTs were fabricated within an array of channels, achieving precise intertube spaces of 10.4 nm (Fig. 5a). Using the SHINE assembly method, Zhao et al. [56] then created a multichannel p-channel metal-oxide semiconductor field-effect transistor (FET) by fixing the DNA-templated CNTs onto a polymer-templated silicon wafer. The CNTs were fixed into position with metal bars, and then, electrodes and gate dielectrics were deposited onto the device (Fig. 5b). The relatively poor electronic performance often observed with biotemplating was remedied by removing contaminating DNA and metal ions with ultra-pure water, low-concentration H2O2, and thermal annealing after the CNT fixing stage. This rinsing-after-fixing approach improved the key transport performance metrics by a factor of 10 compared to the previous biotemplated FETs. This approach highlights the advantage of using DNA origami for the organization of truly three-dimensional architectures.
4 The Future of DNA-Organized Electronics
The future of DNA-organized electronics will likely resemble its past and present but will build on substantive technical advances that fall outside the field. The key enabler, the ability to organize and ultimately design structure at the atomic scale, will be augmented by new opportunities for using novel mechanisms to mediate electron flow. In particular, it should be possible to either make DNA itself more conductive by changing its fundamental chemistry, or to better adapt biocompatible electronic materials to nanostructured DNA scaffolds.
4.1 Making DNA More Electronic
While there are now extremely interesting opportunities for creating Schottky junctions between DNA-patterned and non-DNA-patterned materials, as described above, the opportunities for atomic scale control over the geometry and charge flow, as envisioned by Seeman [2] remains largely unrealized to-date. The key to further enablement may come through the control of chemistry that is afforded by DNA nanotechnology. It is relatively simple to append electronic elements (the most obvious being ferrocene) to nucleobases, allowing more precise control over where electron transfer occurs. Further, the introduction of unnatural nucleobases offers further opportunities for atomic level placement, including non-standard base-pairs that specifically chelate metals at the Watson–Crick interface [57].
4.2 Scaffolding Biocompatible Electronic Materials
While the electronic properties of native DNA can be improved, it is still somewhat surprising that it is a conductive material at all, given the lack of obvious redox moieties available [58]. Recently, there has been a paradigm shift (entirely in the Kuhnian sense) in our understanding of how biological materials can potentially transfer electrons. The intermediacy of redox active compounds remains a key feature of bio-enabled electrochemistry and has been successfully utilized in constructing photonic DNA-organized excitonic circuits [59,60,61,62]. However, the opportunities for long distance electron transfer in the absence of such intermediacy are becoming more and more apparent. This has long been the case for tunneling between organic cofactors in cytochrome couples (for example) but has only recently been implicated for peptides and proteins that lack cofactors.
A particularly relevant example of this shift in understanding has been garnered from the study of a synthetic 29-mer peptide that forms an antiparallel coiled-coil hexamer (ACC-Hex) and has been shown to have a remarkably high electrical conductivity [63]. The mechanism of electron transport is currently under debate, since features of both ohmic electronic transport and metallic-like temperature dependence are observed, despite the fact that it contains neither extended conjugation, π-stacking, nor redox centers. A similar story seems to be unfolding in the study of electrically conductive protein nanowires (e-PNs). Geobacter sulfurreducens, a common anaerobic species of bacteria found in anoxic subsurface sediments, is capable of respiring via the reduction of metals, such as Fe(III). These bacteria are able to accomplish this feat by producing long thin filaments that protrude from the cell and electronically link the cell to the metal [64]. Similar to the ACC-Hex fibers, purified e-PNs display ohmic electronic transport and metallic-like temperature dependence. They also contain a high density of aromatic amino acids positioned conservatively throughout one of their constituent proteins [65]. Removal of the aromatic amino acids drastically reduces the electrical conductivity of the nanowires [64].
The potentially critical role of aromatic amino acids in electronic conduction presents a conundrum about what novel electron transport mechanisms may be available to biological polymers. Irrespective of the underlying physics, there has been a remarkable plethora of practical devices produced from the e-pili [66,67,68], including generating energy from environmental ambient humidity [69]. Currently, these methods involve using thin-film approaches to create devices, and as we have seen in other aspects of microelectronics, this can ultimately limit the overall device architecture and functionality. As with other electronic components, such as CNTs, the use of DNA origami now offers a truly unique opportunity to contort and position these conductive wires into specific orientations (Fig. 6). However, the potential for developing sophisticated devices goes well beyond CNTs, since a variety of properties in the pili can be tuned via genetics: They can be functionalized with peptide domains to bind specifically to sites on DNA nanostructures, going beyond the terminal attachment of carbon nanotubes; the number and type of aromatic residues available for conductance can be modulated at will; the length and diameter of the pili can be controlled biologically. The use of DNA origami to organize protein-based nanowires into electrode arrays would represent an entirely new direction in bioelectronics, one which we believe could finally realize the potential of Dennard’s and Moore’s laws at the nanometer-scale.
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Walker, D.J.F., Szmuc, E.R., Ellington, A.D. (2023). Organizing Charge Flow with DNA. In: Jonoska, N., Winfree, E. (eds) Visions of DNA Nanotechnology at 40 for the Next 40 . Natural Computing Series. Springer, Singapore. https://doi.org/10.1007/978-981-19-9891-1_8
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