Abstract
Essentially, all motion in living organisms emerges from the collective action of biological molecular machines transforming chemical energy, originally harvested from light, into ordered activity. As a man-made counterpart to nature’s biomolecular machines, chemists have created artificial molecular machines that display controlled and even directional motion in response to light. However, to be of practical value, the motion of these light-fuelled molecular machines will have to be coupled to the rest of the world. Inspired by the complex functional movement seen in the plant and animal world, chemists have undertaken the challenge to harness molecular motion and, so, they have set artificial molecular motors and switches to work and perform useful mechanical action at the macroscopic level. Here, we review these recent developments. We show how modern research has embraced the full complexity of the molecular world by aiming at the design of autonomous, and sometimes adaptive, molecular systems that work continuously under the effect of illumination. We report evidence that molecular motion can be engineered into highly sophisticated movements and that, from a fundamental point of view, continuous movement can only emerge when man-made molecules cooperate, in space and time. Eventually, unravelling the rules of molecular motion will support the creation of molecular materials that produce work continuously under a constant input of energy.
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References
Herzog, W. Skeletal Muscle Mechanics: From Mechanisms to Function. (Wiley, Chichester, UK, 2000).
Jarrell, K. F. & McBride, M. J. The surprisingly diverse ways that prokaryotes move. Nat. Rev. Microbiol. 6, 466–476 (2008).
Teyssier, J., Saenko, S. V., van der Marel, D. & Milinkovitch, M. C. Photonic crystals cause active colour change in chameleons. Nat. Commun. 6, 6368 (2015).
Stern, C. D. Gastrulation: From Cells to Embryo. (Cold Spring Harbor Laboratory Press, New York, 2004).
Zhang, L., Marcos, V. & Leigh, D. A. Molecular machines with bio-inspired mechanisms. Proc. Natl Acad. Sci. U. S. A. 115, 9397–9404 (2018).
Browne, W. R. & Feringa, B. L. Making molecular machines work. Nat. Nanotechnol. 1, 25–35 (2006).
Kay, E. R. & Leigh, D. A. Rise of the molecular machines. Angew. Chem. Int. Ed. 54, 10080–10088 (2015).
Abendroth, J. M., Bushuyev, O. S., Weiss, P. S. & Barrett, C. J. Controlling motion at the nanoscale: rise of the molecular machines. ACS Nano 9, 7746–7768 (2015).
Balzani, V., Credi, A. & Venturi, M. Light powered molecular machines. Chem. Soc. Rev. 38, 1542–1550 (2009).
Balzani, V., Credi, A., Raymo, F. M. & Stoddart, J. F. Artificial molecular machines. Angew. Chem. Int. Ed. 39, 3348–3391 (2000).
Erbas-Cakmak, S., Leigh, D. A., McTernan, C. T. & Nussbaumer, A. L. Artificial molecular machines. Chem. Rev. 115, 10081–10206 (2015).
Peplow, M. The tiniest Lego: a tale of nanoscale motors, rotors, switches and pumps. Nature 525, 18–21 (2015).
Kassem, S. et al. Artificial molecular motors. Chem. Soc. Rev. 46, 2592–2621 (2017).
Feringa, B. L. The art of building small: from molecular switches to motors (Nobel lecture). Angew. Chem. Int. Ed. 56, 11060–11078 (2017).
Leigh, D. A. Genesis of the nanomachines: the 2016 Nobel Prize in Chemistry. Angew. Chem. Int. Ed. 55, 14506–14508 (2016).
Kholodenko, B. N. Cell-signalling dynamics in time and space. Nat. Rev. Mol. Cell Biol. 7, 165–176 (2006).
Novák, B. & Tyson, J. J. Design principles of biochemical oscillators. Nat. Rev. Mol. Cell Biol. 9, 981–991 (2008).
Astumian, R. D. Design principles for Brownian molecular machines: how to swim in molasses and walk in a hurricane. Phys. Chem. Chem. Phys. 9, 5067–5083 (2007).
Astumian, R. D., Mukherjee, S. & Warshel, A. The physics and physical chemistry of molecular machines. ChemPhysChem 17, 1719–1741 (2016).
Garcia-Garibay, M. A. Crystalline molecular machines: encoding supramolecular dynamics into molecular structure. Proc. Natl Acad. Sci. U. S. A. 102, 10771–10776 (2005).
Uchida, K., Nishimura, R., Hatano, E., Mayama, H. & Yokojima, S. Photochromic crystalline systems mimicking bio-functions. Chem. Eur. J. 24, 8491–8506 (2018).
Naumov, P., Chizhik, S., Panda, M. K., Nath, N. K. & Boldyreva, E. Mechanically responsive molecular crystals. Chem. Rev. 115, 12440–12490 (2015).
Khuong, T.-A. V., Nuñez, J. E., Godinez, C. E. & Garcia-Garibay, M. A. Crystalline molecular machines: a quest toward solid-state dynamics and function. Acc. Chem. Res. 39, 413–422 (2006).
Irie, M., Fukaminato, T., Matsuda, K. & Kobatake, S. Photochromism of diarylethene molecules and crystals: memories, switches, and actuators. Chem. Rev. 114, 12174–12277 (2014).
Kobatake, S., Takami, S., Muto, H., Ishikawa, T. & Irie, M. Rapid and reversible shape changes of molecular crystals on photoirradiation. Nature 446, 778–781 (2007).
Koller, D. & Van Volkenburgh, E. The Restless Plant. (Harvard University Press, Cambridge, MA, 2011).
Hofhuis, H. et al. Morphomechanical innovation drives explosive seed dispersal. Cell 166, 222–233 (2016).
Hatano, E. et al. Photosalient phenomena that mimic Impatiens are observed in hollow crystals of diarylethene with a perfluorocyclohexene ring. Angew. Chem. Int. Ed. 56, 12576–12580 (2017).
Medishetty, R. et al. Single crystals popping under UV light: a photosalient effect triggered by a [2+2] cycloaddition reaction. Angew. Chem. Int. Ed. 53, 5907–5911 (2014).
Zhu, L., Al-Kaysi, R. O. & Bardeen, C. J. Reversible photoinduced twisting of molecular crystal microribbons. J. Am. Chem. Soc. 133, 12569–12575 (2011).
Aspuru-Guzik, A. et al. Charting a course for chemistry. Nat. Chem. 11, 286–294 (2019).
Gennes, P. G. de. & Prost, J. The Physics of Liquid Crystals. (Clarendon Press, Oxford, 1993).
Kleman, M. & Lavrentovich, O. Soft Matter Physics: An Introduction. (Springer, New York, 2004).
Eelkema, R. & Feringa, B. L. Amplification of chirality in liquid crystals. Org. Biomol. Chem. 4, 3729–3745 (2006).
Kitzerow, H. & Bahr, C. Chirality in Liquid Crystals. (Springer-Verlag, New York, 2001).
Liu, D. & Broer, D. J. Liquid crystal polymer networks: preparation, properties, and applications of films with patterned molecular alignment. Langmuir 30, 13499–13509 (2014).
White, T. J. & Broer, D. J. Programmable and adaptive mechanics with liquid crystal polymer networks and elastomers. Nat. Mater. 14, 1087–1098 (2015).
Ryabchun, A., Li, Q., Lancia, F., Aprahamian, I. & Katsonis, N. Shape-persistent actuators from hydrazone photoswitches. J. Am. Chem. Soc. 141, 1196–1200 (2019).
Bandara, H. M. D. & Burdette, S. C. Photoisomerization in different classes of azobenzene. Chem. Soc. Rev. 41, 1809–1825 (2012).
Schultz, T. et al. Mechanism and dynamics of azobenzene photoisomerization. J. Am. Chem. Soc. 125, 8098–8099 (2003).
Tsutsumi, O., Shiono, T., Ikeda, T. & Galli, G. Photochemical phase transition behavior of nematic liquid crystals with azobenzene moieties as both mesogens and photosensitive chromophores. J. Phys. Chem. 101, 1332–1337 (1997).
Matczyszyn, K. & Sworakowski, J. Phase change in azobenzene derivative-doped liquid crystal controlled by the photochromic reaction of the dye. J. Phys. Chem. B 107, 6039–6045 (2003).
Liu, D. & Broer, D. J. Liquid crystal polymer networks: switchable surface topographies. Liq. Cryst. Rev. 1, 20–28 (2013).
Ikeda, T., Mamiya, J. & Yu, Y. Photomechanics of liquid-crystalline elastomers and other polymers. Angew. Chem. Int. Ed. 46, 506–528 (2007).
Ube, T. & Ikeda, T. Photomobile polymer materials with crosslinked liquid-crystalline structures: molecular design, fabrication, and functions. Angew. Chem. Int. Ed. 53, 10290–10299 (2014).
Yu, Y., Nakano, M. & Ikeda, T. Directed bending of a polymer film by light. Nature 425, 145–145 (2003).
Zhao, Y. & Ikeda, T. Smart Light-Responsive Materials: Azobenzene-Containing Polymers and Liquid Crystals. (Wiley, Hoboken, NJ, 2009).
Priimagi, A. et al. Location of the azobenzene moieties within the cross-linked liquid-crystalline polymers can dictate the direction of photoinduced bending. ACS Macro Lett. 1, 96–99 (2011).
Dong, L. & Zhao, Y. Photothermally driven liquid crystal polymer actuators. Mater. Chem. Front. 2, 1932–1943 (2018).
Lahikainen, M., Zeng, H. & Priimagi, A. Reconfigurable photoactuator through synergistic use of photochemical and photothermal effects. Nat. Commun. 9, 4148 (2018).
Pei, Z. et al. Mouldable liquid-crystalline elastomer actuators with exchangeable covalent bonds. Nat. Mater. 13, 36–41 (2014).
Darwin, C. & Darwin, F. The Power of Movement in Plants. (Cambridge University Press, Cambridge, 2009).
Isnard, S., Cobb, A. R., Holbrook, N. M., Zwieniecki, M. & Dumais, J. Tensioning the helix: a mechanism for force generation in twining plants. Proc. R. Soc. B Biol. Sci. 276, 2643–2650 (2009).
Mahadevan, L. & Matsudaira, P. Motility powered by supramolecular springs and ratchets. Science 288, 95–100 (2000).
Armon, S., Efrati, E., Kupferman, R. & Sharon, E. Geometry and mechanics in the opening of chiral seed pods. Science 333, 1726–1730 (2011).
Elbaum, R. & Abraham, Y. Insights into the microstructures of hygroscopic movement in plant seed dispersal. Plant Sci. 223, 124–133 (2014).
Iamsaard, S. et al. Conversion of light into macroscopic helical motion. Nat. Chem. 6, 229–235 (2014).
Iamsaard, S. et al. Preparation of biomimetic photoresponsive polymer springs. Nat. Protoc. 11, 1788–1797 (2016).
Aßhoff, S. J. et al. High-power actuation from molecular photoswitches in enantiomerically paired soft springs. Angew. Chem. Int. Ed. 56, 3261–3265 (2017).
Purcell, E. M. Life at low Reynolds number. Am. J. Phys. 45, 3–11 (1977).
van Oosten, C. L., Bastiaansen, C. W. M. & Broer, D. J. Printed artificial cilia from liquid-crystal network actuators modularly driven by light. Nat. Mater. 8, 677–682 (2009).
Wani, O. M., Verpaalen, R., Zeng, H., Priimagi, A. & Schenning, A. P. H. J. An artificial nocturnal flower via humidity-gated photoactuation in liquid crystal networks. Adv. Mater. 31, 1805985 (2019).
Wani, O. M., Zeng, H. & Priimagi, A. A light-driven artificial flytrap. Nat. Commun. 8, 15546 (2017).
Martin, N. et al. Light-induced dynamic shaping and self-division of multipodal polyelectrolyte-surfactant microarchitectures via azobenzene photomechanics. Sci. Rep. 7, 41327 (2017).
Chen, J. et al. Artificial muscle-like function from hierarchical supramolecular assembly of photoresponsive molecular motors. Nat. Chem. 10, 132–138 (2017).
Koumura, N., Zijlstra, R. W. J., van Delden, R. A., Harada, N. & Feringa, B. L. Light-driven monodirectional molecular rotor. Nature 401, 152–155 (1999).
Koumura, N., Geertsema, E. M., Meetsma, A. & Feringa, B. L. Light-driven molecular motor: unidirectional rotation controlled by a single stereogenic center. J. Am. Chem. Soc. 122, 12005–12006 (2000).
Pollard, M. M., Klok, M., Pijper, D. & Feringa, B. L. Rate acceleration of light-driven rotary molecular motors. Adv. Funct. Mater. 17, 718–729 (2007).
van Leeuwen, T., Lubbe, A. S., Štacko, P., Wezenberg, S. J. & Feringa, B. L. Dynamic control of function by light-driven molecular motors. Nat. Rev. Chem. 1, 0096 (2017).
Camacho-Lopez, M., Finkelmann, H., Palffy-Muhoray, P. & Shelley, M. Fast liquid-crystal elastomer swims into the dark. Nat. Mater. 3, 307–310 (2004).
Sfakiotakis, M., Lane, D. M. & Davies, J. B. C. Review of fish swimming modes for aquatic locomotion. IEEE J. Ocean. Eng. 24, 237–252 (1999).
Palagi, S. et al. Structured light enables biomimetic swimming and versatile locomotion of photoresponsive soft microrobots. Nat. Mater. 15, 647–653 (2016).
Wie, J. J., Shankar, M. R. & White, T. J. Photomotility of polymers. Nat. Commun. 7, 13260 (2016).
Rus, D. & Tolley, M. T. Design, fabrication and control of soft robots. Nature 521, 467–475 (2015).
Rogóz˙, M., Zeng, H., Xuan, C., Wiersma, D. S. & Wasylczyk, P. Light-driven soft robot mimics caterpillar locomotion in natural scale. Adv. Opt. Mater. 4, 1689–1694 (2016).
Zeng, H., Wani, O. M., Wasylczyk, P. & Priimagi, A. Light-driven, caterpillar-inspired miniature inching robot. Macromol. Rapid Commun. 39, 1700224 (2018).
Goujon, A. et al. Bistable [c2] daisy chain rotaxanes as reversible muscle-like actuators in mechanically active gels. J. Am. Chem. Soc. 139, 14825–14828 (2017).
Iwaso, K., Takashima, Y. & Harada, A. Fast response dry-type artificial molecular muscles with [c2] daisy chains. Nat. Chem. 8, 625–632 (2016).
Takashima, Y. et al. Expansion–contraction of photoresponsive artificial muscle regulated by host–guest interactions. Nat. Commun. 3, 1270 (2012).
Li, Q. et al. Macroscopic contraction of a gel induced by the integrated motion of light-driven molecular motors. Nat. Nanotechnol. 10, 161–165 (2015).
Foy, J. T. et al. Dual-light control of nanomachines that integrate motor and modulator subunits. Nat. Nanotechnol. 12, 540–545 (2017).
Semenov, S. N. et al. Rational design of functional and tunable oscillating enzymatic networks. Nat. Chem. 7, 160–165 (2015).
Grzybowski, B. A. & Huck, W. T. S. The nanotechnology of life-inspired systems. Nat. Nanotechnol. 11, 585–592 (2016).
van Roekel, H. W. H. et al. Programmable chemical reaction networks: emulating regulatory functions in living cells using a bottom-up approach. Chem. Soc. Rev. 44, 7465–7483 (2015).
Smith, M. L., Slone, C., Heitfeld, K. & Vaia, R. A. Designed autonomic motion in heterogeneous Belousov–Zhabotinsky (BZ)-gelatin composites by synchronicity. Adv. Funct. Mater. 23, 2835–2842 (2013).
Buskohl, P. R. & Vaia, R. A. Belousov-Zhabotinsky autonomic hydrogel composites: regulating waves via asymmetry. Sci. Adv. 2, e1600813 (2016).
Sasaki, S., Koga, S., Yoshida, R. & Yamaguchi, T. Mechanical oscillation coupled with the Belousov−Zhabotinsky reaction in gel. Langmuir 19, 5595–5600 (2003).
Yoshida, R. Self-oscillating gels driven by the Belousov–Zhabotinsky reaction as novel smart materials. Adv. Mater. 22, 3463–3483 (2010).
Gelebart, A. H. et al. Making waves in a photoactive polymer film. Nature 546, 632–636 (2017).
White, T. J. et al. A high frequency photodriven polymer oscillator. Soft Matter 4, 1796–1798 (2008).
Katsonis, N., Lacaze, E. & Ferrarini, A. Controlling chirality with helix inversion in cholesteric liquid crystals. J. Mater. Chem. 22, 7088–7097 (2012).
Morrow, S. M., Bissette, A. J. & Fletcher, S. P. Transmission of chirality through space and across length scales. Nat. Nanotechnol. 12, 410–419 (2017).
Eelkema, R. et al. Nanomotor rotates microscale objects. Nature 440, 163–163 (2006).
Bosco, A. et al. Photoinduced reorganization of motor-doped chiral liquid crystals: bridging molecular isomerization and texture rotation. J. Am. Chem. Soc. 130, 14615–14624 (2008).
Eelkema, R. et al. Rotational reorganization of doped cholesteric liquid crystalline films. J. Am. Chem. Soc. 128, 14397–14407 (2006).
Aßhoff, S. J. et al. Time-programmed helix inversion in phototunable liquid crystals. Chem. Commun. 49, 4256–4258 (2013).
Orlova, T. et al. Revolving supramolecular chiral structures powered by light in nanomotor-doped liquid crystals. Nat. Nanotechnol. 13, 304–308 (2018).
Fischer, P., Nalson, B. D. & Yang, G.-Z. New materials for next-generation robots. Science Robotics 3, eaau0448 (2018).
Boulatov, R. The challenges and opportunities of contemporary polymer mechanochemistry. ChemPhysChem 18, 1419–1421 (2017).
Anderson, L. & Boulatov, R. Polymer mechanochemistry: a new frontier for physical organic chemistry. Adv. Phys. Org. Chem. 52, 87–143 (2018).
Akbulatov, S. et al. Experimentally realized mechanochemistry distinct from force-accelerated scission of loaded bonds. Science 357, 299–303 (2017).
Davis, D. A. et al. Force-induced activation of covalent bonds in mechanoresponsive polymeric materials. Nature 459, 68–72 (2009).
Acknowledgements
The authors acknowledge funding support from the European Research Council (Consolidator Grant Morpheus 30968307) and the Netherlands Organization for Scientific Research (Projectruimte grant 13PR3105).
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F.L. and A.R. contributed equally to the manuscript. N.K. directed the project. All the authors contributed to the design, writing and editing of the article.
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Glossary
- Artificial molecular machines
-
Man-made molecules or molecular systems that perform useful tasks by converting an energy input into a mechanically relevant motion.
- Feedback loops
-
Effects that regulate a molecular signal, in space and time. This signal can be a mechanical signal, an electrical signal, an optical signal or, more classically, a concentration of molecules. The regulation mechanism can be based on a network of chemical reactions or on a series of mechanical events.
- Liquid crystals
-
Molecules and materials that exhibit a liquid-crystalline state in specific conditions of temperature or dilution. The liquid-crystalline state is a consequence of molecular shape anisotropy and is characterized by a fluidity that is inherent to conventional liquids, combined with a long-range molecular orientation that is also found in crystals. This long-range organization can occur in solution (lyotropic phases) or in bulk materials (thermotropic phases).
- Gels
-
Colloidal networks, polymer networks or supramolecular assemblies that are expanded throughout their whole volume (e.g. swollen) by a fluid and exhibit no flow when in the steady state.
- Filter effect
-
The effect that limits the propagation of light through the thickness of a molecular material, by absorption or by scattering.
- Photosalient effect
-
Accumulation of stress in bulk materials under continuous irradiation that leads to the abrupt release of kinetic energy via bursting, jumping, rolling, etc.
- Liquid-crystal networks
-
Materials in which the physical properties of polymeric networks and high anisotropy inherent to the liquid-crystalline state are combined.
- Nematic liquid crystals
-
Liquid crystals in which the long axes of the molecules align, on average, in one direction preferentially. This direction is defined as the director n (see Box 1).
- Cholesteric liquid crystals
-
Liquid crystals in which the molecules are organized into a helix.
- Photothermal effect
-
The production of heat by the dissipation of energy, when light is absorbed by molecules in solution or by a molecular material. When coupled to anisotropic media, the increase of temperature can result in the generation of an anisotropic, mechanical strain.
- Planar alignment
-
The situation in which the long axes of the liquid-crystal molecules align parallel to the interface.
- Homeotropic alignment
-
The situation in which the long axes of the liquid-crystal molecules align perpendicularly to the interface.
- Supramolecular polymers
-
Polymers whose monomeric units hold together via highly directional and reversible, non-covalent interactions, including hydrogen bonding, π–π interaction, metal coordination and host–guest interaction.
- Out of equilibrium
-
Description for processes that occur under a constant input of energy and, thus, remain away from thermodynamic equilibrium.
- Negative feedback loop
-
A regulation mechanism by which the increase in the concentration of a product inhibits its own production.
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Lancia, F., Ryabchun, A. & Katsonis, N. Life-like motion driven by artificial molecular machines. Nat Rev Chem 3, 536–551 (2019). https://doi.org/10.1038/s41570-019-0122-2
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DOI: https://doi.org/10.1038/s41570-019-0122-2
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