Biotribology inspires new technologies

Abstract

This review deals with natural biotribological systems and how they
have inspired novel micro- and nanotechnological applications. The
biogenic devices presented here have functional units in the micro- and
nanometer regime and have been evolutionarily optimized over millions
of years. The examples discussed comprise natural micromechanical
systems made of nanostructured silica (diatoms produce hinges and
interlocking devices on the micrometer scale and below), adhesive
molecules (selectin and integrin) that can switch states and account
for white blood cell rolling in endothelial cells, dry adhesives as they
occur on the Gecko foot and certain insect attachment pads, and
single molecules that serve as strong self-healing adhesives (diatom
underwater adhesives, abalone shell proteins).

Full text

Page 1

ISSN:1748 0132 © Elsevier Ltd 2007
Biotribology inspires
new technologies
This review deals with natural biotribological systems and how they
have inspired novel micro- and nanotechnological applications. The
biogenic devices presented here have functional units in the micro- and
nanometer regime and have been evolutionarily optimized over millions
of years. The examples discussed comprise natural micromechanical
systems made of nanostructured silica (diatoms produce hinges and
interlocking devices on the micrometer scale and below), adhesive
molecules (selectin and integrin) that can switch states and account
for white blood cell rolling in endothelial cells, dry adhesives as they
occur on the Gecko foot and certain insect attachment pads, and
single molecules that serve as strong self-healing adhesives (diatom
underwater adhesives, abalone shell proteins).
Ille C. Gebeshuber
Institut fuer Allgemeine Physik, Vienna University of Technology, Wiedner Hauptstrasse 8-10/134, 1040 Wien, Austria
Austria & Austrian Center of Competence for Tribology AC2T, Viktor Kaplan-Strasse 2, 2700 Wiener Neustadt, Austria
E-mail: ille@iap.tuwien.ac.at
All organisms face tribological challenges. Surfaces in relative
motion occur, for example, in joints, in the blinking of an eye, or a
fetus moving in a mother’s womb. While humans have researched
the field of tribology for several thousand years, nature has been
producing lubricants and adhesives, as well as optimizing materials
and junctions, for millions of years.
Biotribologists gather information about biological surfaces in
relative motion, their friction, adhesion, lubrication, and wear, and
apply this knowledge to technological innovation as well as to the
development of environmentally sound products.
Ongoing miniaturization of technological devices such as hard-
disk drives and biosensors increases the necessity for a fundamental
understanding of tribological phenomena at the micro- and nanometer
scale1–3. In micro- and nanotribology, at least one of the two
interacting surfaces in relative motion has a relatively small mass, and
the interaction occurs mainly under lightly loaded conditions. In this
situation, negligible wear occurs and the surface properties dominate
the tribological performance4. Biological systems also excel at this scale
and might serve as templates for developing the next generation of
tools based on nano- and micrometer scale technologies5.
Materials found in nature combine many inspiring properties
such as sophistication, miniaturization, hierarchical organizations,
resistance, and adaptability. The hydrodynamic, aerodynamic, wetting,
and adhesive properties of natural materials are remarkable and often
OCTOBER 2007 | VOLUME 2 | NUMBER 5
30

Page 2

Biotribology inspires new technologies REVIEW
OCTOBER 2007 | VOLUME 2 | NUMBER 5
31
converge on limited constituents or principles. Elucidating those
selected by evolution allows for the development of more reliable,
efficient, and environment-respecting materials6.
Another recurring feature in natural systems is the high
level of integration: miniaturization, the object of which is to
accommodate maximum elementary functions in a small volume;
hybridization between inorganic and organic components to optimize
complementary possibilities and functions; and hierarchy.
However, the thermal and hydrolytic sensitivities of biological
materials limit their applicability in many important synthetic materials
applications. Secondly, organisms cannot choose the materials they
use, but are subject to phylogenetic restrictions (i.e. they have to
pertain to evolutionary history). A real breakthrough requires an
understanding of the basic building principles of living organisms and
a study of the chemical and physical properties at the interfaces, to
control the form, size, and compaction of objects6.
Life itself is still a miracle. Organisms are open complex systems
riding on a trajectory far away from the thermal energy minimum.
Engineers and materials scientists can learn by watching, imitating,
understanding, and generalizing natural approaches to challenges.
The new technology we build in the future should be recyclable and
sustainable, reliable and energy efficient. By elucidating the delicate
and intricate assembly of living organisms, it will be possible to create
new materials and systems.
The following sections focus on four biological examples with
amazing tribological properties. Diatoms are algae just a couple of
micrometers in size that have rigid surfaces in relative motion and
have evolved self-healing adhesives, nanostructured amorphous silica
surfaces, and interconnected junctions7. White blood cells serve as the
police of the body's immune system. They flow in the blood stream
and have to be stopped at the site of an inflammation. An exquisite
arrangement of different, switchable adhesives enables controlled
deployment of anti-inflammatory agents in our bodies8. The Gecko
can easily climb up walls and run on ceilings. The measurement of
the adhesive force exerted by a single Gecko hair9 has opened a
new field of research: dry adhesives. Tough underwater adhesives
produced by diatoms10 and the molecular mechanistic origin of the
‘glue’ responsible for the high fracture resistance of the abalone shell11
conclude the biological examples.
These and other natural systems show great potential as model
systems for innovations in micro- and nanotechnology. This review will
describe some of the first devices based on bioinspired materials:
• A diatom-based sensor for nitric oxide gas;
• A technique for cell separation inspired by the selectin/integrin
complexes;
• Some devices inspired by the Gecko’s foot, such as wall-climbing
robots; and
• Artificial hierarchical, as well as novel, adhesives.
Biotribological model systems
Diatoms – creators of glass castles
Diatoms are unicellular microalgae with a cell wall consisting of a
siliceous skeleton enveloped by a thin organic case7. The cell walls of
each diatom form a pillbox-like shell consisting of two parts that fit
within each other. These microorganisms vary greatly in shape, ranging
from box-shaped to cylindrical; they can be symmetrical as well as
asymmetrical and exhibit an amazing diversity of nanostructured
frameworks7,12 (Figs. 1–3).
Fig. 1 Scanning electron microscopy (SEM) images of the diatom species Amphitetras antidiluvianum Ehrenburg. The sample was obtained from seaweed in Point
Dume State Park, California. The whole cell can be seen in (a). The other images are close-ups of this cell. Scale bars: 20 μm (a), 1 μm (b), 5 μm (c), and 1 μm (d).
(Reproduced with permission. © M. A. Tiffany.)
(a)
(c)
(b)
(d)

Page 3

REVIEW Biotribology inspires new technologies
OCTOBER 2007 | VOLUME 2 | NUMBER 5
32
Diatoms are found in both freshwater and marine environments,
as well as in damp soils and on moist surfaces. They are either free
floating (planktonic forms) or attached to a substrate (benthic forms)
via biogenic adhesives, and some species may form chains of cells
of varying lengths. Individual diatoms range in size from 2 μm up to
several millimeters, although only a few species are larger than
200 μm. Diatoms as a group are very diverse, with 12 000 to 60 000
species reported12,13.
Diatoms can serve as model organisms for micro- and
nanotribological investigations14–16 and as templates for novel three-
dimensional microelectromechanical systems (MEMS)17,18. In ambient
conditions, these organisms produce nanostructured amorphous silica
surfaces. Some diatom species have rigid parts that in relative motion
act like rubber bands when elongated and subsequently released,
whereas other diatom species have evolved strong, self-healing
underwater adhesives10. Diatoms are small, mostly easy to cultivate,
highly reproductive, and, since many of them are transparent, are
accessible using optical microscopy methods.
The discussion of tribologists and nanotechnologists with
diatomists started some years ago. No sign of wear has ever been
found on diatom shells19. In 1999, Parkinson and Gordon20 pointed
out the potential role of diatoms in nanotechnology via designing and
producing specific morphologies. In the same year, at the 15th North
American Diatom Symposium, Gebeshuber and coauthors21 introduced
atomic force microscopy and spectroscopy to the diatom community
as new techniques for in vivo investigations of diatoms. These scanning
probe techniques not only allow for the imaging of diatom topology,
but also for the determination of physical properties like stiffness and
adhesion10,22–26. A representative example of the fruitful exchanges in
the area of diatom nanotechnology can be found elsewhere27.
Some diatom species are even capable of active movement.
Examples of this are Pseudo-nitzschia sp. and Bacillaria paxillifer (the
former name of this diatom is Bacillaria paradoxa because of its
unusual behavior, Fig. 3). B. paxillifer shows a remarkable form of
gliding motility: entire colonies of 5–30 cells actively move through
the water by rhythmical expansion and contraction of the whole cell
colony. The single cells glide against each other – as it seems – in
coordination28. Anomalously viscous mucilage excreted through a
fissure that covers much of the cell length may provide the means for
the cell-to-cell attachment29.
Hinges and interlocking devices in diatoms are very stable and can
still be seen in fossil deposits millions of years old. In 2006, Gebeshuber
and Crawford17,18 presented scanning electron microscopy (SEM)
images of extinct and recent diatom species with linking structures
Fig 2. SEM images of an Eocene fossil (45 million years old) from a deposit at Mors, Denmark. (b) and (c) show the linking structures in more detail. Scale bars:
20 μm, 5 μm, and 5 μm, respectively. The sample is from the Hustedt Collection in Bremerhaven, Germany, # E1761. (Reproduced with permission. © F. Hinz and
R. M. Crawford.)
Fig. 3 Light microscopy images of Bacillaria paxillifer. The single cells, which
are about 100 μm long, slide against each other (see inset). The movement
goes from a stack of cells (a) to an elongated band (b), back to the stack, and
then to an elongation once more. Movies on B. paxillifer motion can be found
on the internet. (Part (a) Reproduced with permission. © Wim van Egmond,
http://www.micropolitan.org. Part (b) Reproduced with permission.
© Y. Tsukii, http://protist.i.hosei.ac.jp/. Inset is author's own work.)
(b) (a)
(c)
(b)
(a)

Page 4

Biotribology inspires new technologies REVIEW
OCTOBER 2007 | VOLUME 2 | NUMBER 5
33
with the aim of showing a correlation between structure and function.
Fig. 2 shows four connections of two Solium exsculptum sibling cells
that lived 45 million years ago and are still in good condition.
Perhaps we might even soon be able to evolve the kind of
nanostructures we want and replicate them in large numbers via the
way diatoms naturally replicate – cell division: a compustat30,31 could
monitor diatom properties and selectively destroy cells that do not
evolve in the desired direction. In this way, directed evolution is taking
place. This conveyor belt-type production could yield nanostructures
for use in technological applications.
Switchable adhesives
The understanding of adhesives on the molecular level is important
for engineering tailored synthetic adhesives. Depending on the
application, either increased adhesion or effective anti-adhesive
mechanisms are necessary. For example, nanorobots floating in the
blood stream, acting as microsurgeons, should not aggregate and
must therefore exhibit strong nonadhesive properties with regard to
the environment32. On the other hand, good adhesive interaction of
implant surface with surrounding tissue is a necessity. Furthermore,
implants should not cause immune reactions via the generation of
small wear particles33.
The interaction of white blood cells with blood vessels shows
adaptive adhesion features. Physiologically, white blood cells help to
defend the body against infectious disease and foreign materials as
part of the immune system. There are normally between 4 x 109 and
11 x 109 white blood cells in a liter of healthy adult blood. The size of
a white blood cell is about 10–20 μm. White blood cells are capable of
active amoeboid motion, a property that allows their migration from
the blood stream into tissue34.
White blood cells in the circulation may stop at a particular site as
a result of interactions with the layer of cells that lines the blood vessel
walls (the endothelium) or the subendothelial matrix35.
Traditionally, the endothelium is thought to be specialized to resist
adhesive interactions with other cells. However, such interactions
do occur during certain important biological events like blood cell
migration through the blood vessel to the site of inflammation. Further
details of these interactions can be found elsewhere36.
White blood cell adhesion to the endothelium plays a central role
in inflammation. Adhesion molecules on the white blood cells and
the endothelium regulate cell interactions during this process. The
adhesion of white blood cells is mediated by adhesion molecules and
also by the force distribution present in the blood vessel37. The specific
molecular mechanisms of adhesion often vary with the local wall shear
stress38,39. Shear stress is a measure of the force required to produce
a certain rate of flow of a viscous liquid and is proportional to the
product of shear rate and blood viscosity. Physiological levels of venous
and arterial shear stresses range between 0.1–0.5 Pa and 0.6–4 Pa,
respectively.
Initially, white blood cells move freely along with the blood stream.
White blood cell adaptive adhesion involves a cascade of adhesive
events40 commonly referred to as initial tethering, rolling adhesion (an
adhesive modality that enables surveillance for signs of inflammation),
firm adhesion, and escape from blood vessels into tissue8 (Fig. 4).
After initial tethering, white blood cells may detach back into the free
stream or begin to roll in the direction of the blood flow37. Their rolling
velocity is typically 10–100 times lower than a nonadherent white
blood cell moving next to the vessel wall.
The rolling velocity is not constant and the cells tend to speed up
and slow down as they roll along the endothelium. At some point,
the white blood cell may become activated, i.e. adheres firmly to the
endothelium, and might migrate through the blood vessel to the site of
inflammation.
Lawrence and coworkers39,41,42 have examined white blood cell
adhesion to certain endothelial cells under well-defined flow conditions
in vitro. The initial flow studies were followed by many further studies
both in vitro43–47 and in vivo48–51, which clearly distinguish separate
mechanisms for initial adhesion/rolling and firm adhesion/white blood
cell migration.
Research has further shown that in a variety of systems, selectin/
carbohydrate interactions are primarily responsible for initial adhesion
and rolling, and firm adhesion and white blood cell migration are
mediated primarily by integrin/peptide interactions (at the site of
inflammation)52.
Integrins are the most sophisticated adhesion molecules known.
They can be found, for example, on the surface of a white blood
cell. In less than a second, signals from other receptors on the cell
are transmitted to its integrin extracellular domains, which undergo
Fig. 4 White blood cell adhesion to the endothelium. (a) No adhesion: the
cells contact the surface but do not bind. (b) Transient adhesion mediated by
selectin molecules: the cells bind very briefly and then lose contact again.
(c) Rolling adhesion mediated by selectin molecules: cells bind and translate
along the surface at a reduced velocity compared with bulk fluid velocity.
(d) Firm adhesion mediated by integrin molecules: the cells bind strongly
to the surface and move at a very slow rate. (Blue: selectin; yellow: selectin
ligand; red: integrin receptor; green: integrin ligand.) (Adapted from8.)
(b)
(a)
(c)
(d)

Page 5

REVIEW Biotribology inspires new technologies
OCTOBER 2007 | VOLUME 2 | NUMBER 5
34
conformational movements (changes in their molecular arrangement)
that enable ligand binding (i.e. the adhesives switch from a
nonadhesive to an adhesive state). These unique, switchable adhesives
rapidly stabilize contacts between white blood cells in the bloodstream
and the endothelium at sites of inflammation53.
Characterization of the molecular and cellular properties that enable
such a transient form of adhesion (which would be of interest for a
variety of technological applications, e.g. for grippers) under the high
forces experienced by cells in blood vessels has been investigated by a
multitude of groups, experimentally as well as theoretically53–58.
In inflammation, firm adhesion can be mediated by activated
integrins once the white blood cells have been slowed by selectin
mediated rolling42,50. Integrins can also mediate firm adhesion when
activated59,60 and may, through conformational changes, mediate both
‘firm’ and ‘transient’ types of adhesion.
The question arises: what functional properties of these molecules
control the different dynamics of adhesion? There is evidence that
the dynamics of adhesion are coded by the physical chemistry of
adhesion molecules, and not by cellular features such as deformability,
morphology, or signaling61,62. Possible physicochemical properties
that give rise to the various dynamic states of adhesion are rates of
reaction, affinity, mechanical elasticity, kinetic response to stress,
and length of adhesion molecules. Adhesion is also dependent on the
magnitude of the force applied to the cells.
Gecko attachment pads
The Gecko is an amazing animal. It can rapidly climb up vertical glass
surfaces, it can climb on ceilings. Microscopy shows that the Gecko
foot (Fig. 5) has about 14 400 hairs (setae) per square millimeter,
covered with even smaller projections only hundreds of nanometers
in diameter. The adhesive force of a single Gecko foot-hair is 600-fold
greater than that of frictional measurements of the material. On the
other hand, highly orientated setae reduce the detachment force of the
foot by simply detaching above a critical angle with the substratum9.
There is strong evidence that the adhesion force in the Gecko is
mediated via van der Waals interactions63.
The Gecko foot also exhibits self-cleaning properties. Autumn and
coworkers64 have found that the self-cleaning effect is simply a result
of the attraction for dirt being slightly less than for the surface on
which the Gecko is walking. This results in a net cleaning effect. Their
mathematical models suggest that self-cleaning in Gecko setae is a
result of geometry not chemistry, thereby opening up the possibility of
constructing synthetic self-cleaning adhesives from a wide variety of
materials.
Self-healing adhesives
Diatoms may be free floating or attached to substrates in seawater,
fresh water, or on moist surfaces. Diatoms have evolved adhesives
that can mediate stable and strong attachment in wet environments10.
There are even diatom species that attach to ice via ice-binding
proteins65. Understanding natural adhesives such as the ones produced
by diatoms opens up opportunities to tailor new synthetic adhesives
for specific applications.
Atomic force spectroscopy investigations of the adhesives certain
diatoms produce to attach to surfaces have shown a multimodular
structure and self-healing behavior10,21. As Dugdale and coworkers66
Fig. 5 The Gecko foot shows a hierarchical adhesive system. (a) Gecko climbing a glass surface. (Photograph courtesy of M. Moffett). (b) Gecko foot. (Photograph
courtesy of M. Moffett). (c) Microstructure of the Gecko foot. There are about 14400 hairs (setae) per square millimeter. (d) and (e) show the nanostructure of
the Gecko foot: each single Gecko seta has hundreds of tiny spatular tips. (Photograph reproduced with permission from K. Autumn and S. Scherf.)
(b) (a)
(e)
(c)
(d)