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Sensors and Actuators B: Chemical
journal homepage: www.elsevier.com/locate/snb

Bacterial sheet-powered rotation of a micro-object
Masaru Kojima a,∗ , Tatsuya Miyamoto a , Masahiro Nakajima b , Michio Homma f ,Tatsuo Arai g , Toshio Fukuda c,d,eaDepartment of Micro-Nano Systems Engineering, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8603, Japan
Center for Micro-Nano Mechatronics, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8603, Japan
Institute for Advanced Research, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, JapandFaculty of Science and Engineering, Meijo University, 1-501, Shiogamaguchi, Tenpaku-ku, Nagoya 468-8502, JapaneIntelligent Robotics Institute, School of Mechatronic Engineering, Beijing Institute of Technology, 5 South Zhongguancun Street, Haidian District, Beijing,
100081, Chinaf
Department of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-Ku, Nagoya 464-8602, Japang
Division of Systems Science, Department of Systems Innovation, Graduate School of Engineering Science, Osaka University, 1-3, Machikaneyama-cho,
Toyonaka 560-8531, Japanbca r t i c l e

i n f oArticle history:
Received 23 February 2015
Received in revised form 11 July 2015
Accepted 16 July 2015
Available online xxx
Keywords:
Biomotor
Bacteria
Surface swarming
Micro-object
Bioactuatora b s t r a c t
Recently, there have been numerous reports of the use of microbes as bio-actuators. In particular, bacteria
are one of the promising candidates for bioactuator development, because of which they have garnereda lot of interest lately. In this paper, we developed a new system for the transport of a micro-object byusing surface swarming Vibrio alginolyticus, a marine bacterium, and achieved high-speed movementof the micro-object. First, we conﬁrmed if YM19 and YM19cheY, two genetic variant strains of V. alginolyticus that are appropriate for surface swarming, were able to transport microbeads. We found that thetransport speed of YM19cheY was higher than that of YM19, and this conﬁrmed high validity of genetic
modiﬁcation. We further tried to control the movement by constructing a microwall and succeeded incausing the rotational transport of the micro-object. Finally, we demonstrated microgear rotation witha rotational speed that was about 7 rpm, thus conﬁrming the effectiveness of our proposed method.
© 2015 Elsevier B.V. All rights reserved.

1. Introduction
Micro-nano-robots and bio-MEMS are well-studied systems
with extensive applications in medicine [1]. To engineer a micronano-robot that can move in blood vessels, it is necessary toengineer an actuator for driving it. A micro-nano-actuator is also
required as a built-in mechanical factor in bio-MEMS. The components are required for engineering a micro-nano-actuator include(i) a mechanical and electrical factor, (ii) a biological macromolecule including protein [2], and (iii) a living organism itself[3–12]. Biological macromolecules and living organisms work asvery small and highly effective actuators, because they utilize
chemical energy instead of electromotive force. Thus, these bioactuators are being touted as “Next Generation Motivity.” Despite
the advances in the ﬁeld of bio-actuator research, many problems∗ Corresponding author. Present address at: Division of Systems Science, Department of Systems Innovation, Graduate School of Engineering Science, Osaka University, 1-3 Machikaneyama-cho, Toyonaka 560-8531, Japan. Tel.: +81 6 6850 6367;
fax: +81 6 6850 6367.
E-mail address: kojima@arai-lab.sys.es.osaka-u.ac.jp (M. Kojima).

remain unsolved. For instances, the biological function of the living
component is not well characterized in some cases. Therefore, thedevelopment of an efﬁcient actuator design is important.
Several recent reports describe the construction of bio-actuatorswith microbes. More speciﬁcally, the rotation of microgears bybacteria is one area of extensive research. Some bacteria are ﬂagellated and can swim in aqueous environments by using the ﬂagellaas screws. Flagellar rotation is brought about by a ﬂagellar motor,
which is embedded in the bacterial cell membrane [13–16]. Hiratsuka et al. [10] reported the rotation of microgear by using mobile
Mycoplasma, where the bacteria attached to a microgear directory were pushing the microgear. Further, Sokolov et al. [11] andLeonardo et al. [12] reported that randomly swimming bacteria
could rotate a gear with an asymmetrical shape (ratchet shape).
However, the rotational speed of the microgear in this case waslow (1–2 rpm). Therefore, an improvement of rotational speed wasdesired.
In this study, we have used Vibrio alginolyticus, a gram-negative
marine bacterium. V. alginolyticus is suitable for use in a bioactuator
because this species has some distinct advantages. First, V. alginolyticus has a speciﬁc motile mode known as “Surface swarming”.
This bacteria have two types of ﬂagella, the polar ﬂagellum andhttp://dx.doi.org/10.1016/j.snb.2015.07.071
0925-4005/© 2015 Elsevier B.V. All rights reserved.

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the lateral ﬂagella. The bacteria, rod-shaped swimmer cell, usually swim in aqueous environments using polar ﬂagellum, which
is produced constitutively; however, when the bacterial cells are
introduced in high-viscosity environments such as animal surfaces, they switch to surface swarming [17]. Surface swarming cells
become elongated in shape and generate new peritrichous ﬂagella(lateral ﬂagella) for surface swarming and thus move over the surface. This movement resembles social motility. Actually surface
swarming cells can move on 1.3% agar plate, whereas swimming
cells could not move in this condition. In this motile mode, the characteristics of the motile bacterial sheet (carpet) [18] are different
from those of swimming [11,12] and gliding bacterial cells [9,10],making it a good candidate for use in a bioactuator. We expected
some advantages in this motile mode. (1) It can easily provide a highdensity motile cells (The space is ﬁlled with almost 100% bacteria). (2) High torque is expected because the number of ﬂagellafor one cell also increased. (3) High torque is expected by social
motility like movement of surface swarming cells. Hence, in ourpresent study, we have used bacterial cells in this motile mode as ahigh torque actuator. Second, genetically engineered strains havebeen well established in this species such that the inherent properties of the cells can be exploited (genetic engineering was not
used in the previous report [10–12]). At ﬁrst, the basic property oftransporting the microbeads using the surface swarming propertyof V. alginolyticus was analyzed. Moreover, to achieve high-speed
rotation of the micro-object, to a level that could be achieved for
micro-gears, we aimed to regulate the direction of the transport
and to apply this motion to rotate the micro-object.
2. Materials and methods
2.1. Bacterial strains, growth conditions and media
V. alginolyticus strains used are a polar ﬂagellum-defective
mutant, YM19 (Pof− Laf+ ), YM19cheY, in which the cheY geneis deleted, was constructed by an in-frame deletion in the cheY
gene with homologous recombination. Mean swimming speeds of
YM19 and YM19cheY cells are 15.2 ± 4.1 (␮m/s) and 23.1 ± 6.3(␮m/s), respectively. V. alginolyticus cells were cultured at 30 ◦ C in
VC medium (0.5% polypeptone, 0.5% yeast extract, 0.4% K2 HPO4 , 3%
NaCl, 0.2% glucose), VPG medium [1% polypeptone, 0.4% K2 HPO4 ,
3% NaCl, 0.5% (w/v) glycerol].

was then incubated under isothermal conditions to rid the waferof the template. The fabricated microwall was further observed by
optical and laser microscopy (Fig. 1A and B).
2.4. Regulation of transport using the ratchet-shaped microwall
A culture of the YM19cheY strain was prepared by incubation
at 30 ◦ C for 14 h. Two microliters of this bacterial culture was inoculated onto a 1.3% VPG agar plate and the plates were incubatedat 30 ◦ C for 4 h. After incubation, as in case of the experiment withmicrobeads, microbeads of 1.3 ␮m diameter were introduced tofacilitate observation of the bacterial sheet. The fabricated ratchetshape microwall was then introduced onto the bacterial sheet andobserved using optical microscopy.
2.5. Microwall fabrication by photolithography
The silicon wafer was cleaned by ultrasonic treatment and thenspin coated with SU-8 3010 at 3300 rpm. The spin-coated wafer
was then exposed to a micropattern generator (␮-PG), and thepatterned wafer was developed and used as the template. PDMS
was then poured onto the silicon wafer, which was then incubatedin an isothermal incubator to rid the wafer of the template. After
sufﬁcient hardening of the PDMS, we rid the template from thePDMS. The fabricated microwall was observed by optical and laser
microscopy (Fig. 1C).
2.6. Microgear fabrication by photolithography
A silicon wafer was cleaned by ultrasonic treatment and thenspin-coated with AZ5214E at 500 rpm. A second spin coating was
performed with SU-8 3005 at 7000 rpm. The spin-coated wafer wasthen exposed to a ␮-PG and developed after patterning. The fabricated microgear was then observed by optical and laser microscopy(Fig. 1D).
2.7. Driving the microgear into the microwall
We ﬁrst prepared 9-cm 1.3% VPG agar plates, and streaked asingle colony onto the plate. The plate was then incubated for 6 h
at 30 ◦ C. The microgears were picked up using manipulators andplaced on the bacterial sheet. The microwall was placed on the
microgear, and the setup was observed by optical microscopy.

2.2. Transport of micro-object
3. Results and discussion
The conditions and procedures used in the experiment performed for transporting the microbeads were as follows: 1.3%
VPG agar in 9-cm culture plates. The bacteria were cultured in
VC medium for 14 h at 30 ◦ C. Two microliters of bacteria cultured
overnight was inoculated at the center of the VPG plates. Drying of
the plate such that the liquid was no longer visible was taken as
conﬁrmation that the liquid drop with bacteria had seeped into theplate. These plates were incubated for a few minutes at 30 ◦ C. Afterthe short incubation, 2 ␮l of VPG solution with 10 ␮m (diameter)
microbeads was introduced at the spot of bacterial cell inoculationon the plate. The plates were then incubated for 4 h at 30 ◦ C, after
which the bacteria formed a sheet. The behaviors of the bacterial
cells and the microbeads were observed by optical microscopy.
2.3. Fabrication of a ratchet-shaped microwall
To regulate rational direction, we fabricated a ratchet-shaped
microwall. The method for the fabrication of the microwall was as
described below. The pattern was etched on a silicon wafer using a
focused ion beam (FIB) and this wafer was used as a template. Polydimethylsiloxane (PDMS) was poured on to the silicon wafer, which

3.1. Transport of the micro-object by the bacterial sheet
Well-established genetic engineering techniques are in place
for V. alginolyticus such that the bacterial cells are made amenable
to modiﬁcations of their morphological properties. In this study,
we used a mutant strain of V. alginolyticus, YM19, which constitutively generates lateral ﬂagella for surface swarming. Furthermore,
we detected the cheY gene, which controls the chemotaxis system,
for generating highly motile bacterial cells [19]. The chemotaxis
genes regulate ﬂagellar motor rotation based on environmental
cues from outside the bacterial cell. The CheY protein, which isa response regulator in the chemotaxis system, can regulate ﬂagellar rotation by associating with the ﬂagellar motor directly. In
surface swarming of V. alginolyticus, CheY slows down the rotational speed of the ﬂagellar motor. Therefore, disruption mutantsof the cheY gene move very fast because of the constitutively highspeed rotation of the ﬂagellar motor (Fig. S1). In this case, bacterial
behavior cannot be controlled by environmental stimuli (chemical, thermal, etc.), although the transport ability increases due tohigh-speed movement. To examine whether surface swarming ofPlease cite this article in press as: M. Kojima, et al., Bacterial sheet-powered rotation of a micro-object, Sens. Actuators B: Chem. (2015),
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Fig. 1. Optical microscopy of fabricated ratchet-shaped microwall. Microwall for beads (A), microwall with pillar (B), microgear (C) and microwall for gear (D).

Fig. 2. Trajectory of microbead moved by YM19 (A), (B) and YM19cheY (C), (D) for 15 s. Motion of microbeads is shown as the shaded region in (A) and (C). The trajectoryof the center position is shown in (B) and (D). Mean-square-displacements of the beads on YM19 and YM19cheY are shown in (E). Solid and dashed lines indicate YM19
and YM19cheY, respectively.

V. alginolyticus can aid in the transport a micro-object, we tried
to transport microbeads (polystyrene) by using surface swarming of YM19 and YM19cheY. Optical microscopy indicated thatbeads with 10 ␮m diameters were transported. From this observation, we conﬁrmed the movement of microbeads on the bacterial
sheets of YM19 and YM19cheY. To compare the movements ofthe microbeads on YM19 and YM19cheY, we tracked and constructed a trajectory of microbead movement. Fig. 2 indicates theresult of tracing the movement for 15 s, where the motion of the

microbeads is shown has been shaded (Fig. 2A and C). The trajectoryof the center of mass was calculated by microbeads movement andshown in Fig. 2B and D. The trajectories of both strains seem chaotic,
such that the direction of transport by the bacterial sheet can besaid to be random. The area spanned by the movement of the beadwith YM19cheY is larger than that with YM19. Furthermore, themean-square-displacement of the bead on YM19cheY is clearlyhigher than that on YM19 (Fig. 2E). These results indicate that thetransport speed of YM19cheY is faster than that of YM19. This

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Fig. 3. Counterclockwise rotational movement of the microbeads covered by the CCW ratchet-shaped microwall (A) and its trajectory for 3 rounds (B). Clockwise rotational
movement of the microbead covered by the CW ratchet-shaped microwall (C) and its trajectory for 3 rounds (D).

Fig. 4. Counterclockwise rotational movement of the microbeads covered by the CCW ratchet-shaped microwall with pillar (A) and its trajectory for 3 raps (B). Clockwise
rotational movement of the microbead covered by the CW ratchet-shaped microwall with pillar (C) and its trajectory for 3 raps (D).

phenomenon is consistent with our hypothesis described above.
The microbeads seemed to be transported by the ﬂow caused bybacteria movement and direct pushes by bacteria. However, moving direction of object is same as bacteria motile direction. Detail
generation mechanism of ﬂow by bacteria movement is unknown.
Future studies are needed to reveal that.

3.2. Regulation of the transport of microbeads by theratchet-shaped microwall
To regulate the movement of the microbeads, an asymmetric(ratchet-shaped) microwall was used for controlling the motionof the bacterial sheet. In this experiment, we fabricated two

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5Fig. 5. Rotational movement of microgear in microwall. Results are shown as sequential images (A), the graph of the angular motions for every 1 s (B), and ﬂuctuations inangular velocity plots (C).

differently shaped walls—one clockwise (CW) and one counterclockwise (CCW) ratchet-shaped wall. The results of the observation of the fabricated microwalls by optical microscopy showthat the inner diameter of the ratchet-shape microwall was about
16 ␮m, the external diameter was 24 ␮m, and the depth was about
7.5 ␮m (Fig. 1A shows the result of the 7.5-␮m deep CW).
As the next step, we observed the movement of the microbeads
with the ratchet-shaped microwall. The results for the 7.5-␮m deep
wall are shown in Fig. 3. Fig. S2 shows sequential images of the
movement of a single bacterium for 1.4 s. The movement of thebacterium was random; therefore, at times, the bacterium moved
backwards (see Fig. S2 at 0.44 s). In this case, the bacterium wascaught on to a barb, and then moved forward again (see Fig. S2 at
0.93 s), so that the movement of the bacterium was limited to asingle direction.
Fig. 3A shows CCW rotation of the transported beads as sequential images in 1.0 s (Movie S1). The 1.3-␮m microbeads had a CCW
rotational motion, and this trajectory for 3 rounds is shown in
Fig. 3B. From this result, we were able to calculate the velocity of
microbead movement, and the bead rotated at 48.6 rpm on an average. Fig. 3C shows CW rotation of transported beads. The 1.3 ␮mmicrobeads had a CW rotational motion (Movie S2). From the trajectory data, we calculated the velocity of microbeads and thesebeads rotated at 24.7 rpm on an average (Fig. 3D). Sometimes, themicrobeads crossed the center of the microwall. Therefore, the trajectory and velocity of microbeads was not stable and could not be
precisely calculated.
We attempted to regulate the rotational direction of the
movement of the bacteria by using the microwall. However, therotational movement was not smooth. Microbeads were sometimes
trapped in the barb. To rectify this inconsistency in rotational movement, we fabricated a center pillar in the microwall (Fig. 1B). We
then observed the movement of the microbeads with the ratchetshaped microwall with the pillar. The conditions and the procedureof the experiment were same as in the previous case. The results
are shown in Fig. 4. This time the microbeads were not held up on
the barb and rotated smoothly in the surroundings of the pillar.
Thus, we achieved smooth rotational movement using the pillar.

From this result, the CW rotation speed was 27.9 rpm on an average(Fig. 4B), and the CCW rotation speed was 34.3 rpm on an average(Fig. 4D). The difference in the CW and CCW rotation speeds was
signiﬁcantly reduced.
Consequently, clockwise and counterclockwise rotation wasachieved. Moreover, it was conﬁrmed that the microbeads rotatedon the bacterial sheet. The fractions of the microbeads moving in
the intended directions were almost 100%. The rotation continued
for at least 3 h. However, the rotational speed decreased gradually.
We believe that the decrease in the rotational speed is caused by
the extensive bacterial proliferation near the microwall. After 3 h,there was a signiﬁcant loss of space for movement.
3.3. Driving microgear
To use actuation by bacterial sheet as motor, we fabricatedmicrogears using SU-8 and the microwall using PDMS, and tried
to drive the microgear using the rotational movement of bacteria. Optical microscope image of fabricated microgear is shown in
Fig. 4A. The external diameter of the microgear was 19 ␮m and thethickness was 2 ␮m. The image of the fabricated microwall, as seen
under the optical microscope, is shown in Fig. 4B. The inner diameter of the microwall was 33 ␮m, the diameter of the pillar was
7 ␮m, and the depth was 10 ␮m.
The results are shown as sequential images in Fig. 5A (Movie S3).
From this result, we could estimate the velocity of rotation of the
microgear by image analysis. Fig. 5B shows a graph of the angular motions for every 1 s. This result indicates that the microgear
was stably rotating. The ﬂuctuations can be better appreciated in
the angular velocity plots in Fig. 5C. The microgear showed smaller
ﬂuctuations in angular velocities, compared to that reported previously [11]. Furthremore, the fractions of the microgears moving
in the intended directions were almost 100%. The ratchet-shaped
microwall generated a constant movement of bacteria and regulated bacterial cell number depending on the wall size. Thus, astable rotation of microgear was achieved.
From the calculations, the microgear was found to rotate atabout 7.1 ± 2.2 rpm on an average. The rotation of the microgear

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was signiﬁcantly slower than that of microbeads. The microgear
become slower speed for receiving the larger viscous resistancethan that of microbeads. Furthermore, in the case of microgear, fordisplaced rotational center during the rotation of microgear, there
might be frictional resistance between the central ﬁxed pole andhole of the gear. Therefore, the rotation of the microgear becomesslow. In this case, the linear speed of the edge is about 7.1 ␮m/s,
whereas V. alginolytius could move at approximately 20 ␮m/s. The
circumference of the microgear was about 60 ␮m. Thus, the microgear might rotate at a maximum speed of 20 rpm. This observation
leaves a large margin of improvement with regard to microgear
rotation. Improvements in the experimental conditions might facilitate faster rotation.
4. Conclusions
In the present study directed towards the application of bioactuators, we established a driving system using a bacterial sheet.
First, we succeeded in controlling the rotational direction of bacteria by using a microwall. To use the bacterial sheet as a motor,
we fabricated a microgear and a microwall. We succeeded in driving the microgear into the microwall. Reductions in the size of the
motor toward the micro/nano-meter scale have been hindered byproblems such as the reductions in the sizes of the driving forces
including energy supply systems. Our proposed bio-motor is one
solution to these problems. Furthermore, this system could be used
for the further analysis of bacterial cell properties such as surface
swarming, which are not well studied so far. Therefore, we canﬁnd interesting phenomenon, for example similar to E. coli guiding
movement [20], from this microwall system.
Acknowledgements
This work was partially supported by a Grant-in-Aid for Scientiﬁc Research on Innovative Areas (23106005, 23106006). We
would like to thank S. Kojima for supplying the bacterial sample
and for the helpful discussions, K. Nogawa for help with microfabrication, and K. Sekiyama and H. Fukuoka for the useful discussions.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, inthe online version, at http://dx.doi.org/10.1016/j.snb.2015.07.071.
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Biographies
Masaru Kojima received Doctor of Science degree from Nagoya University in 2006.
He had been a Research Fellow with the Department of Biology, Nagoya University in
2007, Research Fellow on Global Center of Excellence (GCOE) with the Departmentof Biology, Nagoya University in 2008, Assistant Professor on GCOE with the Department of Micro-Nano Systems Engineering, Nagoya University from 2008, AssistantProfessor in Department of Systems Innovation, Osaka University from 2012. His
main research interest is biophysics, in particular, using the biological object andproteins as bio actuator.
Tatsuya Miyamoto received master degree from Nagoya University in 2012. His
research interest is bio-MEMS and micro/nano bio robot.
Masahiro Nakajima received Doctor of engineering degree from Nagoya University.
He had been a Research Fellow of the Ministry of Education, Culture, Sports, Science and Technology, Nagoya University in 2006, Research Associate in Departmentof Micro-Nano Systems Engineering, Nagoya University from 2006, Assistant Professor in Department of Micro-Nano Systems Engineering, Nagoya University from2007, Assistant Professor in Center For Micro-Nano Mechatonics, Nagoya University
from 2009. He has interest in the research ﬁeld of the applications of micro/nanomanipulation, micro/nano-mehanics, nano-biology.
Michio Homma received the Doctor of Science Doctor of Science degrees from
Tokyo University in 1985. During 1985–1988, he was a Postdoctoral Associatewith the Department of Molecular Biophysics Biochemistry, Yale University. During
1988–1992, he was a Lecturer with the Research Institute for Disease Mechanism
and Control, Nagoya University School of Medicine, where he was promoted to an
Associate Professor. During 1992–1998, he moved to the Department of Molecular Biology, Faculty of Science, Nagoya University, Nagoya, Japan, where he has
been a Professor with the Division of Biological Science, Graduate School of Science.
His current research interests include energy transduction and sensory transduction in bacteria, and a special emphasis is put on the supramolecular complexes
located in the cytoplasmic membrane, namely, the ﬂagellar motor and the rhodopsin
complex.
Tatsuo Arai is a Professor at Graduate School of Engineering Science, Osaka University. He is also a project leader of Hyper Bio Assembler for 3D Cellular Innovation,
supported by the Japanese Ministry of Education, Culture, Sports, Science, and Technology. He is specialize in robot mechanism analysis, design, and application. His
research interest also covers micro manipulation system, limb mechanism robot,
tele-operation, and bio-assembly.
Toshio Fukuda received the Doctor of Engineering from the University of Tokyoin 1977. He joined in the National Mechanical Engineering Laboratory, in Japan,
from 1977. He joined in the Science University of Tokyo in Japan from 1982. He
joined in the Department of Mechanical Engineering, Nagoya University in Japan asa professor from 1989. He joined in the Institute for Advanced Research, Nagoya University, Faculty of Science and Engineering, Meijo University in Japan, and Intelligent
Robotics Institute, School of Mechatronic Engineering, Beijing Institute of Technology in China as a professor from 2013. He is mainly involved in the research ﬁeld ofintelligent robotic and mechatronic system, celler robotic system, micro and nanorobotic system.

Please cite this article in press as: M. Kojima, et al., Bacterial sheet-powered rotation of a micro-object, Sens. Actuators B: Chem. (2015),
http://dx.doi.org/10.1016/j.snb.2015.07.071