Catalytic molecular motors: Fuelling autonomous movement by a surface bound synthetic manganese catalase

Article abstract of DOI:10.1039/b505092h

A molecular approach to the powering of multi-component nano-devices capable of autonomous translational and rotational motion through the conversion of chemical to kinetic energy is reported. The Royal Society of Chemistry 2005.

Full text of DOI:10.1039/b505092h

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Catalytic molecular motors: fuelling autonomous movement by a
surface bound synthetic manganese catalase{
Javier Vicario, Rienk Eelkema, Wesley R. Browne, Auke Meetsma, Rene´ M. La Crois and Ben L. Feringa*
Received (in Cambridge, UK) 13th April 2005, Accepted 12th May 2005
First published as an Advance Article on the web 31st May 2005
DOI: 10.1039/b505092h
both the particle dimensions and the ability to localise the
production of O2. The use of a synthetic oxygen evolving complex
might be of considerable advantage to future (non-metallic) micro-
and nanoscale molecular machines, as it can be easily (chemically)
modified, tether length can be adjusted, and local catalyst density is
controllable. Furthermore, it offers the possibility to control
oxygen evolution down at the molecular level. A synthetic
molecular system capable of chemically driven motion still remains
a major hurdle, however, due to the requirement to be able to
immobilise molecular catalysts on particles with retention of
catalyst function. Furthermore the integrity of the multicomponent
system created must not be compromised during the conversion of
chemical to kinetic energy.
A molecular approach to the powering of multi-component
nano-devices capable of autonomous translational and rota-
tional motion through the conversion of chemical to kinetic
energy is reported.
The effective use of nano- and microscale machinery capable of
driving linear and rotary motion is essential to the proper
functioning of living cells.1 The construction of artificial molecular
machines, ubiquitous in nature, remains, however, a major
contemporary challenge.2 The recent development of molecular
based systems including shuttles,3 rotors,4 muscles,5 switches,6
elevators,7 motors8 and processive catalysts9 has brought the
prospect of synthetic molecular based ‘mechanical machines’
within sight. Nevertheless the required ‘fuelling’ of the motion of
these molecular systems remains a major hurdle. Indeed, central to
the function of nanoscopic (e.g. ATP-synthase, which employs H+
gradients) and microscopic (e.g. ATP-driven actin filaments in
muscle tissue, controlled by Ca2+ gradients) molecular devices
employed by nature is the ability to convert chemical to
mechanical energy.1,10 Although light-powered molecular devices,
such as the first molecular motor capable of performing repetitive
unidirectional rotary motion, developed in our group,8a,11 hold
considerable potential towards driving changes in wholly mole-
cular systems, as demonstrated recently in liquid crystal films,12 the
movement of larger assemblies (i.e. 1024–1029 m) requires
concerted action of several molecular motors or significantly
greater power to effect rotational and translational motion. The
high power density required might be achievable through the use
of chemical energy. Indeed Kelly and coworkers8b have demon-
strated that rotary motion can be induced by sequential chemical
conversions. An attractive alternative to the application of
complex chemical transformations to drive molecular based
devices is provided by the approach taken recently by the groups
of Whitesides,13 Sen, Mallouk and Crespi,14 and Ozin and
Manners,15 in which the decomposition of H2O2 on the surface
of microscopic composite (bi-)metallic objects is employed to
achieve translational and/or rotational movement through the
creation of localised [O2] gradients. The nature of the motion
induced by this approach was found to be critically dependent on
Here, we report our preliminary results on autonomous
movement of microparticles (m-particles) via a [covalently] tethered
synthetic catalase mimic. The design (Fig. 1) of a molecular based
device capable of converting chemical energy to kinetic energy,
comprises three key elements: an object (micro- or nanoparticle,
complex or macro-molecule) to be transported, a spacer/tether and
a catalyst for converting chemical energy to kinetic energy. The
new highly efficient catalase mimic, [(Mn(II)(L2))2(RCO22)]+ (1)
(where HL is 2-{[[di(2-pyridyl)methyl](methyl)amino]methyl}phe-
nol) developed within our group, is well suited to such a role. Its
high rate of disproportionation of H2O2 to H2O and O2 (i.e.
catalase activity) and the ability to attach the catalyst covalently,
through either the ligand L2 or more promisingly the bridging
carboxylate group, allows for facile fixation to the surface of nano-
and micro-scale objects through chemical modification.
Designed as a functional model for dinuclear Mn-catalase
enzymes,16 ligand HL, bearing a phenol, tertiary amine and two
pyridine binding sites, was synthesised. Complexation with
Mn(ClO4)2 in the presence of carboxylic acids provided dinuclear
MnIIMnII-complexes 1a and 1b (Scheme 1). X-ray analysis of
the benzoate complex 1a confirms the bridging nature of the
phenolates and the carboxylate (Fig. 2, see also ESI{).17 The ability
of 1 to catalyse H2O2 disproportionation was demonstrated in
several solvents18 with turn over frequencies (T.O.F.) of y0.27 s21
at 25 uC (i.e. CH3CN, 30% aq. H2O2).
Department of Organic and Molecular Inorganic Chemistry, Stratingh
Institute, University of Groningen, Nijenborgh 4, 9747 AG, Groningen,
The Netherlands. E-mail: B.L.Feringa@rug.nl
{ Electronic supplementary information (ESI) available: detailed experi-
mental procedures for the synthesis of the ligand and complexes,
spectroscopic and electrochemical data, observation of the moving
particles and time videos representing the dynamic behaviour are shown
as photographs (Fig. 3, 4) in this paper. See http://www.rsc.org/suppdata/
cc/b5/b505092h/
Fig. 1 Design of a system propelled by a catalase mimic.
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Covalent immobilisation of the catalyst via the bridging
carboxylate ligand was achieved using the p-formyl-functionalised
complex 1b, which was attached to aminopropyl-modified silica
microparticles (40–80 mm) in ethanol–acetonitrile through imine
formation (Scheme 2). Multiple rigorous washing steps (EtOH,
CH3CN, CH2Cl2 and Et2O) of the m-particles were performed to
remove residual, non-covalently bound, complex 1b. The mod-
ification of the m-particles via an imine bridge was confirmed by IR
spectroscopy and electrochemistry (see ESI{), through comparison
of the aminopropyl-functionalised particles, its iminobenzoic acid
analogue, and the particles functionalised with 1b as well as free
complex. The immobilised catalytic system obtained was found
to be robust to detachment (i.e. retains activity, IR and redox
properties are unaffected, see ESI{) from the m-particles and
exhibited high activity towards H2O2 disproportionation as
observed with the free catalyst (e.g. 1a). The modified particles
were recoverable by filtration and could be recycled several times
without significant loss in activity. The characteristic imine
absorption at 1645 cm21 is not affected by H2O2 decomposition
and IR spectra of functionalised m-particles are unaffected by
catalase activity. Kinetic and thermodynamic parameters of H2O2
decomposition by functionalised m-particles as well as free complex
1b (5 wt%) were obtained by Eyring plot analysis,19 showing first
order kinetics (w.r.t. [H2O2]) with large negative entropy of
activation (ku 5 3.09 6 1023 s21, DS{ 5 2288.62 J K21mol21
Scheme 1
for the free complex 1b and ku 5 1.51 6 1023 s21, DS{
2291.07 J K21mol21 for the 1b-functionalised microparticles).
5
In order to study the movement induced by O2 formation, a thin
liquid film, containing a dilute suspension (in CH3CN or glycerol)
of the 1b-functionalised m-particles, mixed with non-functionalised
m-particles (40–80 mm) as reference, on a microscope glass slide,
were monitored after addition of a 5% H2O2 solution in CH3CN.
O2 evolution was observed as small O2 bubbles appearing on only
the catalyst-functionalised m-particles. Both linear and rotary
Fig. 2 X-ray structure of 1a.
Scheme 2
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mechanism by which propulsion of the particles takes place (recoil
from O2 bubbles,13 interfacial tension gradient14) and the
parameters governing the dynamics of the system need further
investigation. The principle introduced here, to use a designed
molecular catalyst to induce motion, is currently explored in the
controlled motion of nanoparticles and functional molecules.
The authors thank the (WRB) Dutch Economy, Ecology,
Technology (EET) program and the (JV) Departamento de
Educacio´n, Universidades e Investigacio´n del Gobierno Vasco for
financial support.
Notes and references
1 Molecular Motors, ed. M. Schliwa, Wiley-VCH, Weinheim, 2002.
2 M. Venturi, A. Credi and V. Balzani, Molecular Devices and Machines –
A Journey into the Nanoworld, Wiley-VCH, Weinheim, 2003.
3 (a) A. R. Pease, J. O. Jeppesen, J. F. Stoddart, Y. Luo, C. P. Collier and
J. R. Heath, Acc. Chem. Res., 2001, 34, 433; (b) R. Ballardini, V. Balzani,
A. Credi, M. T. Gandolfi and M. Venturi, Acc. Chem. Res., 2001, 34,
445; (c) C. M. Keaveney and D. A. Leigh, Angew. Chem. Int. Ed., 2004,
43, 1222.
Fig. 3 Pathway of an 80 mm 1b-functionalised SiO2 particle in CH3CN
and its position at a) 0 s, b) 4 s, c) 14 s and d) 18 s (see supplementary
movie{).
4 (a) Z. Dominguez, T.-A. V. Khuong, H. Dang, C. N. Sanrame,
J. E. Nunez and M. A. Garcia-Garibay, J. Am. Chem. Soc., 2003, 125,
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5 M. C. Jime´nez, C. Dietrich-Buchecker and J.-P. Sauvage, Angew. Chem.
Int. Ed., 2000, 39, 3284.
Fig. 4 Rotational movement of an 80 mm 1b-functionalised SiO2 particle
in glycerol and its position at a) 0 s and b) 45 s.
6 Molecular Switches, ed. B. L. Feringa, Wiley-VCH, Weinheim, 2001.
´
7 J. D. Badjic, V. Balzani, A. Credi, S. Silvi and J. F. Stoddart, Science,
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motion of the modified m-particles was found. The translational
motion of a m-particle (see movie in ESI{) and the trajectory
followed until the supply of H2O2 is insufficient to sustain
movement, is seen in Fig. 3. The measured average speed for this
8 (a) N. Koumura, R. W. J. Zijlstra, R. A. van Delden, N. Harada and
B. L. Feringa, Nature, 1999, 401, 15; (b) T. R. Kelly, H. De Silva and
R. A. Silva, Nature, 1999, 401, 150; (c) D. A. Leigh, J. K. Y. Wong,
F. Dehez and F. Zerbetto, Nature, 2003, 424, 174.
9 P. Thordarson, E. J. A. Bijsterveld, A. E. Rowan and R. J. M. Nolte,
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particle is 35 mm s21
.
As the dinuclear Mn-complex 1b is a highly active catalyst for
H2O2 decomposition large disturbance of the dispersed film and
numerous collisions of m-particles are observed at higher H2O2
concentrations. The direction of the movement is in accordance
with that of the system of Whitesides and coworkers, with O2
evolution at the trailing end of the moving objects.13 The non-
symmetric nature of the particle with respect to defects capable of
causing cavitation and hence bubble formation rather than
inhomogeneous distribution of catalyst is likely to be the dominant
factor in determining the directionality of the motion induced.
Interestingly, the autonomous moving m-particles also pass along
static particles (Fig. 3b,c) on the surface, changing directionality.
Slow rotational movement of a functionalised m-particle can
also be observed in the more viscous solvent glycerol (Fig. 4).
The measured rotational speed for the depicted particle is 1.55 6
1022 rad s21. As for translational motion, the occurrence of a
catalytically driven autonomous rotary motion (clockwise in the
case illustrated, see ESI{) is attributed to the anisotropy of the
structure with respect to cavitation points. The ability to decouple
[O2] formation with directional control is an important feature of
this approach as it enables directionality and catalyst activity to be
addressed separately.
10 (a) J. E. Walker, Angew. Chem. Int. Ed., 1998, 37, 2308; (b) L. Stryer,
Biochemistry, 4th edition, W. H. Freeman and Co., New York.
11 B. L. Feringa, Acc. Chem. Res., 2001, 34, 504.
12 R.A. van Delden, N. Koumura, N. Harada and B.L. Feringa, Proc.
Natl. Acad. Sci. USA, 2002, 99, 4945.
13 R. F. Ismagilov, A. Schwartz, N. Bowden and G. M. Whitesides,
Angew. Chem. Int. Ed., 2002, 41, 652.
14 (a) W. F. Paxton, K. C. Kisler, C. O. Olmeda, A. Sen, S. K. St.Angelo,
Y. Cao, T. E. Mallouk, P. E. Lammert and V. H. Crespi, J. Am. Chem.
Soc., 2004, 126, 13424; (b) J. M. Catchmark, S. Subramanian and
A. Sen, Small, 2005, 1, 202; (c) T. R. Kline, W. F. Paxton, T. E. Mallouk
and A. Sen, Angew. Chem. Int. Ed., 2005, 44, 744.
15 S. Fournier-Bidoz, A. C. Arsenault, I. Manners and G. A. Ozin, Chem.
Commun., 2005, 441.
16 A. J. Wu, J. E. Penner-Hahn and V. L. Pecoraro, Chem. Rev., 2004, 104,
903.
17 Chemical formula: [C45H41Mn2N6O4][ClO4]; M: 939.18 g mol21; Unit
˚
˚
cell dimensions a 5 15.226(2) A (a 5 90u), b 5 12.924(2) A
˚
˚
(b 5 90.157(9)u) , c 5 10.944(2) A (c 5 90u), V 2153.6(6) A; T 130 K;
monoclinic C2; Z 5 2; m (Mo Ka), cm21 5 7.1; wR(F2) 5 0.0778 for
2
4691 reflections with Fo ¢ 0 and R(F) 5 0.0303 for 4481 reflections
with Fo ¢ 4.0 s(Fo) and 375 parameters, Flack parameter
(X) 5 0.428(15). CCDC number 268595. See http://www.rsc.org/
suppdata/cc/b5/b505092h/ for crystallographic data in CIF or other
electronic format.
18 CH2Cl2, MeOH, CH3CN and glycerol were tested and gave satisfactory
results.
19 O2 evolution was measured in time using the gas burette method
according to A. I. Unuchukwu and P. B. Mshelia, J. Chem. Ed., 1985,
62, 809.
In conclusion, we describe the first molecular-based system in
which catalytic conversion of chemical to mechanical energy
induces autonomous movement of micro-sized particles. The exact
3938 | Chem. Commun., 2005, 3936–3938
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