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Controlled Flight of a Biologically Inspired, Insect-Scale Robot

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Controlled Flight of a Biologically Inspired, Insect-Scale Robot REPORTS systems by seamless integration of transcriptor References and Notes by a single signal. Transcriptor-based logic allows logic elements within natural operons). Also, by 1. B. Wang, M. Buck, Trends Microbiol. 20,376(2012). RNA polymerase flow at a single point on DNA to be controlled, in theory, by as many independent separating gate inputs from gate control signals 2. Y. Benenson, Nat. Rev. Genet. 13,455(2012). 3. T. Miyamoto, S. Razavi, R. DeRose, T. Inoue, ACS Synth. Biol. recombinases as needed. and by using a strong input signal modulated by 2,72(2013). 20. J. A. Lewis, G. F. Hatfull, Nucleic Acids Res. 29,2205 an efficient asymmetric terminator, we were able 4. D. R. Burrill, P. A. Silver, Cell 140, 13 (2010). (2001). to demonstrate and quantify signal amplification 5. J. Bonnet, P. Subsoontorn, D. Endy, Proc. Natl. Acad. Sci. 21. W. R. A. Brown, N. C. O. Lee, Z. Xu, M. C. M. Smith, for all gates (Figs. 3 and 4). U.S.A. 109,8884(2012). Methods 53,372(2011). 6. S. Basu, Y. Gerchman, C. H. Collins, F. H. Arnold, 22. B. Canton, A. Labno, D. Endy, Nat. Biotechnol. 26,787 Output signal levels vary within and among R. Weiss, Nature 434,1130(2005). (2008). the gates reported here (Figs. 2 and 3 and figs. S9 7. M. E. Ortiz, D. Endy, J. Biol. Eng. 6, 16 (2012). 23. Materials and methods are available as supplementary and S10), although not more so than existing 8. Y. Y. Chen, M. C. Jensen, C. D. Smolke, Proc. Natl. Acad. materials on Science Online. genetic logic. We believe that most variation Sci. U.S.A. 107,8531(2010). 24. C. Lou, B. Stanton, Y.-J. Chen, B. Munsky, C. A. Voigt, 9. Z. Xie, L. Wroblewska, L. Prochazka, R. Weiss, Y. Benenson, Nat. Biotechnol. 30,1137(2012). arises from differences in RNA secondary struc- Science 333,1307(2011). 25. L. Pasotti, N. Politi, S. Zucca, M. G. Cusella De Angelis, tures well known to influence mRNA stability 10. A. Tamsir, J. J. Tabor, C. A. Voigt, Nature 469,212(2011). P. Magni, PLoS ONE 7,e39407(2012). and translation initiation rates (fig. S15); such 11. T. S. Moon, C. Lou, A. Tamsir, B. C. Stanton, C. A. Voigt, 26. P. Siuti, J. Yazbek, T. K. Lu, Nat. Biotechnol. (2013). variation might be eliminated by using recently Nature 491,249(2012). 27. L. Qi, R. E. Haurwitz, W. Shao, J. A. Doudna, A. P. Arkin, 12. S. Ausländer, D. Ausländer, M. Müller, M. Wieland, Nat. Biotechnol. 30,1002(2012). reported mRNA processing methods (24, 27). M. Fussenegger, Nature 487,123(2012). 28. G. F. Hatfull et al., J. Virol. 86,2382(2012). Further work is also required to realize precise 13. For example, converting a NOR gate repressed by 29. https://biobricks.org/bpa/ level matching across all gates, and directed evo- transcription factors to an OR gate activated by lution of increasingly asymmetric terminators may transcription factors requires changing how proteins Acknowledgments: We thank M. Juul, T. Knight, S. Kushner, C. Smolke, B. Townshend, the Endy and Smolke labs, and be needed to reduce low output levels for most interact with RNA polymerase (from competitive binding and occlusion to recruitment and initiation) the Stanford Shared FACS Facility. Funding was provided gates (fig. S10); additional gate-specific tuning of and simultaneous reworking of the basal activity for by the NSF Synthetic Biology Engineering Research Center, NAND would be required given its noncanonical core promoter elements (from a constitutively active Stanford Center for Longevity, Stanford Bio-X, the logic element. Nevertheless, existing gates al- promoter that can be repressed to a weak promoter Townshend/Lamarre Family Foundation, and the Siebel ready support single-layer programmable digital that does not spontaneously initiate transcription yet Foundation. DNA sequences are available in GenBank that transcription factors activate). (accession nos. KC529324 to KC529332). DNA constructs will logic, control-signal amplification, sequential logic, 14. C. Wadey, I. Deese, D. Endy, “Common signal carriers,” in be made available via Addgene. and cell-cell communication of intermediate logic Adventures in Synthetic Biology (OpenWetWare and on May 3, 2013 Nature Publishing Group New York, 2005), chap. 3; states. Multi-input gates supporting high “fan-in” Supplementary Materials available online at http://hdl.handle.net/1721.1/46337. could be realized by using additional integrases www.sciencemag.org/cgi/content/full/science.1232758/DC1 15. T. S. Ham, S. K. Lee, J. D. Keasling, A. P. Arkin, PLoS ONE Materials and Methods (28)(fig.S16).Transcriptor-basedgatescanalso 3,e2815(2008). Figs. S1 to S15 likely be directly combined with other logic fam- 16. A. E. Friedland et al., Science 324,1199(2009). Appendices S1 to S4 17. P. A. Varadarajan, D. Del Vecchio, IEEE Trans. ilies to expand the power of engineered genetic References (30–44) Nanobioscience 8,281(2009). computers. All logic gates and uses thereof dem- Movie S1 onstrated or disclosed here have been contributed 18. J. Bardeen, W. Brattain, Phys. Rev. 74,230(1948). 19. With transistor-based logic, gates use a base, emitter, 14 November 2012; accepted 13 March 2013 to the public domain via the BioBrick Public and collector architecture that classically only allows Published online 28 March 2013; Agreement (29). for control of electrical current at one point on a wire 10.1126/science.1232758 www.sciencemag.org ventional technologies for macroscale aircraft Controlled Flight of a Biologically propulsion and manufacturing are not viable for millimeter-scale robots because of inefficiencies that arise from force scaling, suggesting a biolog- Inspired, Insect-Scale Robot ically inspired solution based on flapping wings Kevin Y. Ma,*† Pakpong Chirarattananon,† Sawyer B. Fuller, Robert J. Wood (7–9). Here, we report an aggregation of inno- Downloaded from vations in design, manufacturing, actuation, and Flies are among the most agile flying creatures on Earth. To mimic this aerial prowess in a similarly control to create an insect-scale flying robot—a sized robot requires tiny, high-efficiency mechanical components that pose miniaturization challenges robotic fly—that successfully demonstrates teth- governed by force-scaling laws, suggesting unconventional solutions for propulsion, actuation, and ered but unconstrained flight behavior reminis- manufacturing. To this end, we developed high-power-density piezoelectric flight muscles and a cent of flying insects. manufacturing methodology capable of rapidly prototyping articulated, flexure-based sub-millimeter For inspiration of form and function, we used mechanisms. We built an 80-milligram, insect-scale, flapping-wing robot modeled loosely on the Diptera (flies) as a model system because of the morphology of flies. Using a modular approach to flightcontrolthatreliesonlimitedinformationaboutthe relative simplicity of the flight apparatus—flies robot’sdynamics,wedemonstratedtetheredbutunconstrained stable hovering and basic controlled flight by classification have only two wings—and maneuvers. The result validates a sufficient suite of innovations for achieving artificial, insect-like flight. the exemplary aerial agility that they exhibit. Dipteran flight has been well-studied (5, 10–18), sing flapping wings and tiny nervous feats—from sensorimotor transduction to the un- and it is understood that insect wings undergo systems, flying insects are able to per- steady aerodynamics of their wing motions—is acomplextrajectorydefinedbythreerotational Uform sophisticated aerodynamic feats such just beginning to be understood (1–3), aided in degrees of freedom (10). This has been simpli- as deftly avoiding a striking hand or landing on part by simulation (4)andscaledmodels(5). Mo- fied in the robotic fly to a reciprocating flapping flowers buffeted by wind. How they perform these tivated by a desire for tiny flying robots with motion in which the wings’ pitch rotation is reg- comparable maneuverability, we seek to create ulated with passive compliant flexures (19)—an a robotic vehicle that mirrors these basic flight enabling simplification for mechanism design and School of Engineering and Applied Sciences and the Wyss In- stitute for Biologically Inspired Engineering, Harvard Uni- mechanics of flies. At the scale of flies, no such manufacture. Key aspectsoftheoscillatorywing versity, Cambridge, MA 02138, USA. vehicle has been demonstrated to date because motion are the flapping frequency and wing stroke *Corresponding author. E-mail: [email protected] of the severe miniaturization challenges that must amplitude; the robotic fly achieves 120 Hz and †These authors contributed equally to this work. be overcome for an insect-sized device (6). Con- 110°, respectively, similar to the 130-Hz wing beat www.sciencemag.org SCIENCE VOL 340 3 MAY 2013 603 REPORTS frequency and 120°- to 150°-stroke amplitude in lithic, parallel nature of this method facilitates lever arm to amplify the small displacement of flies of comparable mass (1, 11). The wing planform mass production (Fig. 1A) and precision assem- the piezoelectric flight muscle. A second degree is inspired by the aspect ratio and area distribution bly through folding (20). All electromechanical of freedom is wing pitch rotation: This is rele- of the hoverfly Eristalis,withwingareachosen elements of the robotic fly—including flight mus- gated to a passive, elastic flexure hinge at the base to be consistent with similarly sized insects in terms cles, thorax, skeleton, and wings—were manufac- of the wing. Inertial, aerodynamic, and elastic of wing loading and peak wing velocities (1). tured by use of SCM. Structural elements were forces determine wing rotation as it interacts with The mechanical components for a robotic created by using high stiffness-to-weight-ratio the air (Fig. 1F) (19, 23). This passive wing rota- fly require feature sizes between micrometers carbon fiber-reinforced composites, and articu- tion mimics that observed in insects (12), although and centimeters—too large for silicon-based mi- lation was achieved with polyimide film flexure Diptera are known to possess additional muscu- croelectromechanical systems (MEMS) and too hinges emulating low-friction revolute joints.
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