# Magnetic field-enhanced transformation of biochemical energy into motion of enzyme-modified graphene monolayers

Ruchao Gao, Sabrina Bichon, Sébastien Gounel, Gerardo Salinas, Lin Zhang, Nicolas Mano, Alexander Kuhn

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Ruchao Gao, Sabrina Bichon, Sébastien Gounel, Gerardo Salinas, Lin Zhang, et al.. Magnetic field-enhanced transformation of biochemical energy into motion of enzyme-modified graphene monolayers. Chemical Communications, 2025, 61 (75), pp.14410-14413. 10.1039/d5cc03912f. hal-05263604

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Distributed under a Creative Commons CC BY 4.0 - Attribution - International License
Magnetic field-enhanced transformation of biochemical energy
into motion of enzyme-modified graphene monolayers

Received 00th January 20xx,
Accepted 00th January 20xx

DOI: 10.1039/x0xx00000x

Ruchao Gao,ᵃ,ᵇ Sabrina Bichon,ᶜ Sébastien Gounel,ᶜ Gerardo Salinas,ᵇ Lin Zhang,*ᵃ Nicolas Mano,*ᶜ and Alexander Kuhn*ᵃ,ᵇ

This contribution studies enzymatically driven graphene
monolayer swimmers for the direct transformation of biochemical
energy into motion. The swimmers are elaborated via bipolar
electrodeposition of gold and asymmetric immobilization of
glucose oxidase and bilirubin oxidase on small pieces of a
graphene monolayer. Most importantly, we demonstrate that the
speed of the free-standing hybrid objects can be enhanced by an
external magnetic field, allowing also controlled rotation, despite
the absence of ferromagnetic construction elements. These results
illustrate the potential of 2D materials for designing, in synergy
with magnetic fields, original enzyme-based energy conversion
devices.

With the rapid consumption of global energy and growing
environmental problems, the development of sustainable
energy conversion technologies has become one of the central
focuses of scientific research.¹ Energy conversion strategies
based on biological systems have attracted extensive attention
due to their environmental compatibility and renewability.²
For instance, some microbes or enzymes, capable of
converting biomass into commodity chemicals or fuels,
demonstrate significant potential for generating green and
clean energy.³,⁴ Enzyme-powered micro/nano swimmers⁵,
which convert chemical energy directly into mechanical energy,
have become a new direction in the field of energy conversion
due to the use of bio-sourced fuel. Such enzymatically
powered systems typically undergo redox or hydrolysis
reactions, catalysed by single or multiple enzymes (such as
bilirubin oxidase (BOD)⁶, glucose oxidase (Gox)⁷, urease ⁸),
generating local ion concentration gradients and self-
electrophoresis to drive autonomous movement. Compared

with traditional chemical and bubble propulsion systems,
enzymatic swimmers offer distinct advantages. Their fuels
(such as glucose, oxygen or urea) are widely available and of
natural origin, while the reaction products are environmentally
friendly.⁹ Those advantages make them compatible with the
requirements of sustainable energy conversion devices. Thus,
the development and optimisation of such devices is an
ongoing challenge in current research, whether it concerns
their design, the improvement of their speed or a better
directional control. In addition to the often reported micro-
and nanoswimmers¹⁰, macro-scale enzymatic swimmers have
also been studied, using e.g. conductive substrates like carbon
fibers⁵ᵃ,¹¹, or PPy films¹², modified with enzymes, leading to
interesting self-propulsion behaviour.

In this general context, two-dimensional (2D) materials offer
significant potential for developing enzymatic swimmer
systems due to their excellent mechanical properties, high
intrinsic conductivity, and atomic thickness.¹³ To achieve
directed motion, the symmetry of such materials needs to be
broken and one straightforward approach, among many
others¹⁴, is based on bipolar electrochemistry (BPE)¹⁵. Recently,
this versatile technique has been employed to deposit with
high spatial control various metals and polymer composites at
specific sites of monolayer graphene¹⁶, and it therefore can be
advantageously used for designing novel graphene-based
bioelectrochemical swimmers.

In this study, we developed an enzymatic graphene swimmer
by generating first ultrathin gold layers at both extremities of a
piece of monolayer graphene via bipolar electrodeposition.
Then, glucose oxidase and bilirubin oxidase were immobilized
on these oppositely located Au-modified areas (Figure 1A).
These bi-enzymatic hybrid 2D objects exhibit intriguing
dynamic features in the presence of glucose and oxygen. Most
importantly, we show for the first time that by applying an
external magnetic field, their behavior can be precisely
controlled, allowing well-defined rotational motion, combined
with an improved energy conversion efficiency.

<footnote>ª Engineering Research Center for Nanomaterials, Henan University, 475000,
Kaifeng, China. E-mail: lin.zhang@henu.edu.cn</footnote>

<footnote>ᵇ University of Bordeaux, CNRS, Bordeaux INP, ISM UMR 5255, 33600, Pessac,
France. E-mail: kuhn@enscbp.fr</footnote>

<footnote>ᶜ Centre de Recherche Paul Pascal, University of Bordeaux, CNRS, UMR 5031,
Pessac, France. E-mail: nicolas.mano@crpp.cnrs.fr</footnote>

<footnote>Supplementary Information available: See DOI: 10.1039/x0xx00000x</footnote>
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**Figure 1** (A) Illustration of the mediated enzymatic graphene swimmer. Trajectory of an enzymatic graphene swimmer (BOD: Gox = 1: 1) moving at the The graphene monolayer sheets are prepared via a wet-transfer method.¹⁷ Au layers are deposited at both extremities of the graphene sheets by bipolar electrodeposition. As shown in Scheme S1, the graphene sheet is first positioned at the air/water interface of an Au salt solution between two feeder electrodes. When a sufficiently high electric field is applied to the electrolyte, an Au layer is deposited at the cathodically polarized extremity of the graphene sheet. Then the sheet is rotated by 180° and the same electric field is applied to deposit Au at the opposite extremity. Figure S1A displays the optical image of a graphene sheet after Au deposition. A distinct color contrast is observed at the two ends of the monolayer, attributed to the Au deposition, while the middle part of the sheet remains transparent, indicating no metal deposition. Figure S1B and C show the corresponding EDS mapping of the two Au-modified ends, confirming the successful site-specific metal deposition. The bipolar electrodeposition of Au layers on specific areas of graphene provides a better contact between the graphene surface and the enzyme-containing redox polymer. In addition, the extension of the modified area is controllable by adjusting the applied electric field, a feature which can only be achieved by BPE.[15b,c]

The enzymatic graphene swimmer was prepared by immobilizing two enzymes (Gox and BOD) at the opposite extremities of an Au-modified graphene sheet using Os-based redox polymer hydrogels.¹⁸ The enzyme-hydrogel mixtures were site-specifically loaded onto the Au-modified areas via drop-casting (see SI). In the presence of both, glucose and oxygen, the spatially separated enzymatic reactions establish a short-circuited biofuel cell. Gox catalyzes the oxidation of glucose at the anodic side, generating electrons (e⁻, red arrow in Figure 1A) which move through the graphene monolayer to be used for the oxygen reduction reaction mediated by BOD at the cathodic side.

Simultaneously, the glucose oxidation at the anodic side continuously generates protons, while the oxygen reduction at the cathode consumes protons. Consequently, protons are asymmetrically distributed along the graphene layer and

develop a local electric field. This self-generated field causes an electroosmotic fluid flow by proton migration in the electric double layer of the swimmer. This induces a force ($F_E$, orange arrow, Fig 1A) experienced by the graphene swimmer, propelling it in the direction opposite to the proton flux. To validate this self-electrophoresis mechanism, the dynamic behaviour of the enzymatic graphene swimmer was systematically investigated under varying conditions. A first control experiment was carried out in an oxygen-free solution. As in this case no electron transfer is possible, consequently no significant motion is observed besides a small random drift (Figure S2 and Video S1A). In the next set of experiments, an oxygen-saturated 0.1 M phosphate buffer solution (pH 7.0), maintained at 37°C via a water bath and containing 20 mM glucose as fuel, has been employed. As shown in Video S1B, and also illustrated by the trajectory displayed in Figure 1B, the graphene swimmer exhibits a linear propulsion in the direction of the Gox-modified edge with an average speed of 2.7 cm/s. Most interestingly, when an external magnetic field (Figure 1, blue arrow) is imposed on this system, the induced Lorentz force ($F_L$, green arrow in Figure 1), in synergy with $F_E$, results in a complete change of the swimmer's trajectory, despite the absence of magnetic elements in its architecture. We analyzed in more detail the generated circular motion in the first 5 seconds. With the northpole facing up (Figure 1C and Video S1C), a clockwise rotation is observed with an average speed of 2.6 cm/s. In contrast, with the southpole up (Figure 1D, Video S1D), counter clockwise rotation with an average speed of 2.7 cm/s is recorded. Notably, the linear component of the motion is always in the direction of the Gox-modified extremity. The presence of an external magnetic field also creates a magnetohydrodynamic (MHD) flow around the two enzyme spots. This convection can also accelerate the reaction,¹⁹ and thus the energy conversion efficiency. An enhanced linear speed is observed at short times in the presence of the magnetic field with the north pole facing up (Figure S3A), and a similar increase is detected for the south pole-up configuration (not shown). This improvement can be attributed to the generation of a local MHD flow, facilitating the transport of substrate molecules towards both enzyme spots in the early moments of the experiment when the swimmer starts to move. Once swimmer motion is established, this additional MHD-related mass transport has no longer a significant impact on the overall reaction rate and thus the speed.

<figure><img src="image_3.png" /></figure>

To

<figure><img src="image_4.png" /><figcaption>**Figure 2** Initial maximum of angular speed of enzymatic graphene swimmers without magnetic field (grey), with northpole (purple) or southpole up (orange). Error bars</figcaption></figure>
provide a more quantitative analysis of the influence of the
magnetic field on the dynamic behaviour of the swimmers, the
angular displacement and angular speed under different
conditions (no external magnetic field, north pole up, and
south pole up) were analysed using trajectory data extracted
from Videos S1A-C. Figure 2 compares the initial angular speed
of the three experiments after placing the swimmer at the
air/solution interface. In the absence of the external magnetic
field, it exhibits only a neglectable angular speed, due to either
a drift or a slight asymmetry in the shape of the graphene
sheet. When the magnetic field is applied, the angular speed is
193 °/s and 185 °/s for the north pole and south pole-up
configuration, respectively.

The linear and angular speeds of the graphene swimmer not
only depend on the magnetic field, but are also directly
correlated with the efficiency of both redox reactions involving
Gox and BOD, respectively. A critical parameter influencing the
efficiency of the redox reactions is the enzyme loading. All the
above discussed experiments were conducted with the same
enzyme loading ratio (BOD: Gox= 1:1). However, the speed of
the enzymatic graphene swimmer may be limited by the
conversion of oxygen, due to its low solubility, and the
associated consumption of protons by BOD. To address this
aspect, the loading ratio of BOD and Gox was changed to 2:1.
This enhanced BOD loading enables a faster consumption of
the protons and electrons generated by Gox. Consequently,
swimmers with a doubled BOD loading exhibit an average
speed of 3.7 cm/s, a 1.4 times enhancement compared to the
loading ratio of 1:1 under otherwise identical conditions
(Figure 3A, trajectory extracted from Video S2A). Optimization
of the enzyme loading represents therefore an effective
strategy to improve propulsion performance and thus we
further investigated in more detail the motion and angular
speed as a function of this parameter. Figure S3 illustrates the
effects of the magnetic field and varying enzyme loadings. First,
in the case of the same loading of BOD and Gox (black and
green curves in Figure S3A), the speed of both swimmers
gradually decreases and the magnetic field doesn't seem to
have a major impact on the linear speed component, except
for the very beginning of the experiment (vide supra.). In
strong contrast to this, the angular speed component (black
and green curves in Figure S3B) is very sensitive to the
presence of the magnetic field. In the absence of the magnetic
field, the angular speed is close to zero with minor fluctuations.
However, when the magnetic field is applied, the angular
speed is significantly higher. Nevertheless, the angular speed
tends to decrease gradually over time, which is consistent with
the trend of the linear motion. Two reasons might be at the
origin of this behaviour: (1) Initially, the redox polymer
contains dissolved oxygen, so when the swimmer is placed at
the air/solution interface, the enzymes encapsulated in the
redox polymer will consume both, the stored oxygen and
oxygen from the solution. This simultaneous consumption of
oxygen, provided from two sources, results in a temporarily
higher speed. After the oxygen, locally stored in the hydrogel,
is consumed, oxygen from the solution needs to penetrate the
gel to reach the enzyme, and this transport limitation leads to

a gradual decrease of linear and angular speed. (2) The
swimmers move at an initially quite high speed and this
creates rather important shear forces which gradually remove
parts of the enzyme-containing hydrogel as it is facing
downwards and is therefore directly exposed to the strong
local hydrodynamics. Thus, less and less fuel can be converted
per time, inducing a decrease in speed. Unfortunately, this
decrease of activity prevents using the same swimmer several
times. However, we have studied multiple independent
swimmers and observed a very similar dynamic behavior,
indicating a good reproducibility of the protocols. Related to
this aspect, improvements of the life-time might be achieved
by protecting the enzyme layers with membranes.

When the BOD loading is doubled with respect to the amount
of immobilized Gox, linear and angular speed show a
considerable increase (blue curves in Figure S3). This indicates
that oxygen conversion is the rate limiting process and directly
impacts the propulsion efficiency (vide supra.). Also in this case
the speed decreases as a function of time, and it is reasonable

<caption>**Figure 3** (A) Trajectory of an enzymatic graphene swimmer (BOD: Gox = 2: 1) moving at the air/water interface of a O₂ saturated 0.1 M PBS, 20 mM glucose solution, at pH 7 and 37 °C, in the presence of a magnetic field</caption>

with the north pole up. (B) Trajectory of an enzymatic graphene swimmer (BOD: Gox = 2: 1) moving at the air/water interface of a O₂ saturated 0.1 M PBS, 40 mM glucose solution, at pH 5 and 37 °C, in the presence of a magnetic field with the north pole up. (C) Maximum of the initial angular speed of enzymatic graphene swimmers with the north pole-up configuration with different loading ratios between BOD and Gox,

to assume that this is due to a gradual stripping of the redox
hydrogel exposed to strong hydrodynamic forces.

To further enhance the speed of the graphene swimmers, the
composition of the fuel solution can also be optimized. Based
on swimmers with the BOD:Gox= 2:1 loading, the glucose
concentration has been increased from 20 mM to 40 mM, and
the solution pH was adjusted to 5. Under these conditions, the
swimmer shows a significantly improved average linear speed
of 4.8 cm/s (see Figure 3B and Video S2B). Obviously, the
higher glucose concentration can provide more substrate and
thus promote the catalytic activity of Gox, but most
importantly, a pH of 5 is close to the optimal pH of Gox and
BOD, which enhances the activity of both enzymes, thus
strengthening the proton gradient and the resulting
electrophoretic force. The weight of the swimmer is also an
important parameter to achieve high speed. The weight of a
graphene swimmers is around 30 µg, which represents a
unique advantage of using a graphene monolayer as a support.
Besides the linear speed component, the average angular
speed of the enzymatic graphene swimmers is also affected by
the enzyme loading and the composition of the fuel solution.
Figure 3C compares swimmers with different enzyme loading
ratios and after fuel solution optimization. The green bar
represents the initial condition (BOD: Gox = 1: 1) with an
average angular speed of 193 °/s. Doubling the BOD loading
(blue bar, BOD: Gox = 2: 1) improves the average angular
speed to 286 °/s, while further fuel solution optimization (red
bar, 40 mM glucose, pH 5) allows achieving a remarkable
average angular speed of 383 °/s, representing a 100% enhancement compared to the initial condition. The increased BOD loading and the optimization of the composition of the fuel solution amplify both, the proton flux between the two enzyme patches and the electron flow through the graphene sheet. This leads to an enhanced F~E~ and, most importantly, in the presence of the external magnetic field, also to an increase in F~L~. To estimate the power output of such a device, electrochemical measurements were conducted with a classic biofuel cell of analogue composition (Scheme S2). The maximum current density flowing between the bioanode and biocathode reaches 0.35 mA/cm² and a potential difference of 0.32 V (Figure S4). The corresponding initial power output is 0.11 mW/cm² and decreases over time, reaching a smaller but rather stationary value at longer times (Figure S5A). This is in good agreement with the temporal evolution of the swimmer speed (Figure S5B and Video S2B). In addition, the conversion efficiency from electrical to mechanical energy was estimated to be at least 2.4% (see details in the SI).

In conclusion, an enzymatic swimmer has been successfully developed through controlled immobilization of two enzymes on a graphene monolayer. The spatial separation of Gox/BOD patches enables the generation of a proton gradient, triggering autonomous motion with an extremely high speed, reaching up to 6 cm/s after optimization. Most importantly, for the first time we show that the trajectory and speed of such an enzymatic swimmer can be controlled and enhanced by an external magnetic field, allowing for an optimized energy transfer efficiency. This is also made possible, because graphene, as a typical 2D material, offers distinct advantages, including excellent conductivity, flexibility and a high surface area per weight. These proof-of-concept results bridge energy conversion with macroscopic robotics, providing an interesting alternative for biomimetic soft robotic design and targeted delivery applications.

This work has been supported by the National Natural Science Foundation of China (No. 22272044), Natural Science Foundation of Henan Province (232300421079), the Henan center for Outstanding Overseas Scientist (GZS2024004) and the French National Research Agency (ANR) in the frame of the project COOOL (ANR-24-CE07-1874-02). We thank Dr. Sara Grecchi for helping us with some additional experiments.

**Conflicts of interest**

There are no conflicts to declare.

**Data availability**

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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**Table Of Content Figure**
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