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Bioinspired Materials Chemistry II: Biomineralization as Inspiration for Materials Chemistry

Bioinspired Materials Chemistry II: Biomineralization as Inspiration for Materials Chemistry

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BIOINSPIRED MATERIALS CHEMISTRY II



(b)



(c)



(d)



Figure 6.1 Diversity of silica structures from different species of diatoms. (a) Thalassiora pseudonana, scale bar: 1 μm. (b) Coscinodiscus walensii , sacle bar: 5 μm.

(c) Cocconeis species, scale bar: 10 μm. (d) Rimoportula from Thalassiosira weisflogii ,

scale bar: 500 nm. (Adapted with permission. Copyright the American Chemical Society:

Ref. 2.)



particular pattern. To date, synthesis of diatom-like silica structures has not yet

been reproduced in the laboratory.

Bioinorganic iron oxides are formed by a variety of organisms and serve a broad

range of functions, such as iron storage, sensing of magnetic fields, strengthing of

the tissues, and hardening of teeth.1c Some of the well-known and fascinating

forms of iron biomineral are the magnetic nanoparticles composed of magnetite

or greigite that are found in magnetotactic bacteria (Figure 6.2).3 The crystals are

arranged into an intracellular chain of discrete crystals, where each crystal in the



(a)



(b)



(c)



Figure 6.2 (a) Transmission electron microscopy image of a spirilium with a single

chain of cuboctahedral magnetosomes. Scale bar, 1 μm. (b) Chain of magnetite crystals

from a similar type of the magnetotatic bacteria shown in (a). Scale bar, 100 nm. (c) The

intracellular magnetic dipoles of the magnetotatic bacteria allow the cells to align with

the geomagnetic field lines while swimming. Due to the inclination of Earth’s magnetic

field (white arrows), north-seeking bacteria are present in the Northern Hemisphere and

swim toward low oxygen concentrations. South-seeking bacteria in the Southern Hemisphere swim in the opposite direction to fulfill the same goal. (Adapted with permission.

Copyright the American Chemical Society: Ref. 3.)



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chain is located inside a specialized compartment called a magnetosome. It is inside

this intracellular compartment that the magnetite crystals form and align in wellordered chains. Typically, each crystal is 30–140 nm in size, within the single

magnetic domain size range where the particles are highly efficient as a permanent

magnetic carrier. It has been statistically demonstrated that magnetosomes have

crystal size distributions that are narrow, asymmetrical, and negatively skewed

with sharp cutoffs toward larger size and with shape factor consistent for a given

strain.3 Thus, the chain of crystals enables the organism to align itself along the

Earth’s magnetic field, functioning as a navigational device for the alignment along

chemical gradients in aquatic habitats.

Calcium carbonate-based biominerals are the most abundant biogenic minerals

found in Nature. They are especially present in fresh water and marine organisms,

such as sea urchins, sea shells, sponges, and crustaceans but also form gravity

sensors in marine and land animals.1a Calcium carbonate (CaCO3 ) can occur in

the form of three anhydrous crystalline polymorphs—vaterite, aragonite, and calcite; and three hydrated forms—amorphous calcium carbonate (ACC), calcium

carbonate monohydrate, and calcium carbonate hexahydrate. Of these polymorphs,

calcite and aragonite are the most thermodynamically stable forms,4 comprising

the majority of calcium carbonate biominerals.

Various sea shell types contain both calcite and aragonite as a hard part of the

mollusk (Figure 6.3). Generally, the outer prismatic layer of the shell consists of

calcite, and the inner part, nacre, is in the form of plate-like aragonite crystals.5

It is noteworthy, however, that inorganically formed calcite cleaves easily along

the {104} plane and therefore is not very suitable material for protection of the

soft parts of the organism.6 Yet, mollusks are not alone in employing calcite. Sea

urchins, for example, have spicules that are composed of single crystals of calcite

that are several millimeters long and exhibit very smooth surfaces, not corresponding to the well-defined rhombohedral morphology of calcite crystals.6 In order

to enhance the mechanical properties of the calcite crystals and to decrease their

brittleness, proteins are occluded inside the crystal, preferentially in the planes parallel to the c-axis, causing dislocations on the planes that are oblique to the [104]

cleavage planes.6 – 8 The result is an efficient crack deviation mechanism, such that

the spines cleave conchoidally, as if they were composed of glassy materials. This

design strategy essentially introduces anisotropic fracture behavior into a material

that is still highly anisotropic at the atomic level. Thus, mimicking this approach

of occluding polymers inside crystals may well have applications in the field of

materials fabrication. Furthermore, by using amorphous calcium carbonate as a

precursor to calcite, organisms are able to shape the crystals into nearly any desirable morphology.9 As for the aragonitic nacreous layer of sea shells, much of its

mechanical strength derives from its superstructure, where plate-shaped aragonite

crystals ∼500 nm thick are arranged into parallel layers that are separated by a sheet

of organic matrix.10 – 13 This arrangement and combination of organic–inorganic

materials makes the nacre 3000 times tougher than pure inorganic aragonite.

Calcite can also be employed by animals for other purposes besides structural

support and protection. For example, brittlestars use single calcite crystals not



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(a)



(b)



(c)



Figure 6.3 (a) Scanning electron microscopy image of a cross section of the shell of

Atrina rigida, showing the nacreous (white star) and prismatic (white circle) layers. Scale

bar: 10 μm. (b) Scanning electron micrograph of a fracture surface of the cross section

of the nacreous layer. Scale bar: 1 μm. (c) Scanning electron micrograph of the surface

of the prismatic layer. Scale bar: 50 μm. (Adapted with permission. Copyright the Royal

Society of Chemistry: Ref. 14.)



only for skeletal construction but also for specialized photosensory organs.15 The

labyrinthic calcitic skeleton has a regular array of spherical microstructures that

have a characteristic double-lens design. These microlenses are optical elements

that guide and focus the light inside the tissue. The lens array senses the light

from a specific direction; it is generated in order to reduce the spherical aberration

and birefringence. Thus, these animals show photosensitivity from a largely



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light-indifferent behavior to pronounced color change and rapid escape behavior.

They can sense predators at a distance by detecting their shadows and quickly

escape into dark crevices.

Calcium phosphate minerals are known to exist in various compositions, and

the most well-known examples are found in vertebrate bone and teeth. Bone has

unique mechanical properties, defined by its chemical composition and structural

organization (Figure 6.4).16 It is a nanocomposite composed primarily of collagen

type I fibrous matrix that is a scaffold and template, within which carbonated apatite

crystals are embedded.17, 18 The major content of the noncollagenous organic part

consists of highly acidic proteins, which are important to control apatite formation

inside the collagen.19 One of the most interesting characteristics of bone is its hierarchical structure, going from the nanometer to the macroscopic scale (Figure 6.5).16

As such, while all types of bone have the same building block (the mineralized

collagen fibril), arrays of fibrils can be organized in different patterns, generating

a structural diversity that is optimized to functional need. Typical examples are

the woven bone, where fibrils are loosely packed and poorly oriented; the rotated

plywood structure that is common to lamellar bone; arrays of parallel fibers, found

in mineralized tendons; and radial fibril arrays, as found in dentin.16 All these

different arrangements will lead to structures with different mechanical properties.

When looking at the above examples of the level of sophistication found in

biominerals in terms of their adaptation to function, it is no wonder that many

efforts in the fields of chemistry, physics, and materials science have been made in

order to mimic these inspiring structures and their properties. However, controlling

the structure and the morphology of these organic–inorganic composite materials is



Osteon

~100 μm



Lamella

~5 μm



Collagen

molecule

~1.5 nm



Fiber bundle Mineralized

~1 μm

fibril ~100 nm



Mineral

particle

~3 nm

(a)



(b)



(c)



(d)



(e)



(f)



Figure 6.4 Schematic representation of the hierarchical structure of a human femur.

Interfaces at many scales contribute to the extraordinary toughness of bone. (a) Cross

section of a human femur. (b) This image depicts the osteons, which are cylindrical

structures surrounding blood vessels in compact bone. (c) At this level compact bone

consists of lamellae, which can have different architectures according to the type of bone.

(d) The lamellae are built by collagen fibrils aligned parallel to each other. (e) Mineralized

collagen fibril, which consists of collagen type I and crystals of hydroxyapatite. (f) The

crystals of hydroxyapatite are located inside the fibrils, closely associated to the collagen

molecules and oriented with their c-axis along the long axis of the fibril. (Adapted with

permission. Copyright Annual Reviews: Ref. 20.)



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BIOINSPIRED MATERIALS CHEMISTRY II



(b)



(a)



200 μm

(c)



50 μm



(d)



(e)



50 μm



20 μm



Figure 6.5 (a) Optical microscopy image under polarized light of a patterned crystalline

CaCO3 film prepared in the presence of polyacrylic acid. (b) Higher magnification of (a).

(c)–(e) Scanning electron microscopy images of CaCO3 films grown in the presence of

DNA on a poly(caprolactone) scaffold. Panels (d) and (e) show higher magnification of

(c), highlighting the ability of the inorganic coating to follow the contours of the scaffold.

(Panels (a) and (b) reproduced with permission. Copyright Wiley-VCH Verlag GmbH &

Co. KGaA: Ref. 47. Panels (c)–(e) adapted with permission. Copyright the Royal Society

of Chemistry: Ref. 48.)



still a challenge and requires a profound fundamental knowledge of the mechanisms

involved in the biogenic processes.



6.2



LEARNING FROM NATURE



Control over the formation of biominerals occurs at several levels. Most important

is the use of specialized macromolecules, mainly (glyco)proteins and polysaccharides, that are assembled into a three-dimensional (3D) organic matrix framework1a

and provide the microenvironment where mineral deposition occurs.21 Some of

these macromolecules are also occluded inside the mineral phase,6, 8 where they

presumably exert direct control over crystal growth, polymorph type, morphology,

and material properties.22 – 24 Thus, the organic macromolecules form an intimate

mix with the mineral phase at all different hierarchical levels, from the nanometer

to the millimeter scale. In addition, the structure–function relationship between

the different components also plays a significant role,6 first in that it is crucial

for the proper templating of mineral formation, and second, because it determines

the properties of the material as a whole, whether they are mechanical, optical,



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magnetic, and soon. Therefore, these are the concepts that need to be investigated

and applied to the synthesis of materials.

It is very common that, when compared to their geological counterparts, biogenic

crystals possess different morphologies and growth behavior and nucleate from different faces. These differences are clearly due to the directing effect that the organic

phase exerts over the incipient mineral and are among the most intriguing characteristics of biominerals. Generally, acidic macromolecules such as polysaccharides and

(glyco)proteins, which are rich in aspartatic acid or glutamic acid residues and/or

phosphate moieties, are involved in the control over crystal formation, in particular, crystal nucleation.1a Therefore, studies aiming to mimic these templates and to

understand how they induce oriented crystal nucleation have focused on surfaces

having acidic functionalities, such as carboxylic, phosphate, and sulfate groups.

The first synthetic system to investigate crystal nucleation on a synthetic surface

was performed using polyaspartic acid adsorbed on a sulfonated polystyrene film

as a scaffold for calcium carbonate nucleation.22 In this study, oriented nucleation

of calcite was obtained, demonstrating the importance of the ordered arrangement

of the functional groups and the cooperativity between the carboxylates and sulfates in templating calcite nucleation. Subsequently, two other biomimetic systems

were developed: Langmuir monolayers of fatty acids on aqueous subphases25 and

self-assembled monolayers (SAMs) on solid substrates.26 Studies on Langmuir

monolayers were pioneered by Mann et al.,25 who demonstrated the controlled

crystallization of calcium carbonate under monolayers of stearic acid. Further studies on SAMs, which predominantly used functionalized long chain thiols on gold

and silver surfaces, have shown that in addition to the nature of the head group (i.e.,

COO− , –OH, –SO3 − and –PO3 2− ), the organization and orientation of the thiol

chains is important to effectively nucleate calcium carbonate crystals with a high

degree of orientational specificity.27 – 29 These studies show that the stereochemical

and geometrical match between the functional groups in the organic template and

the ions in the organic phase dictates the orientation of the crystal.

A further subject of interest in material science concerns the question of how

to precisely control the morphology of a given mineral. Organisms do this through

two main routes. The first involves the use of water-soluble, generally acidic,

macromolecules, which interact with specific faces of a crystal.23, 30, 31 These

biomolecules may also select a polymorph type either by inhibiting the formation

of the most stable polymorph or by promoting the development of the less stable

forms. The second route is the growth of the mineral within a confined space with

a predefined shape that acts as a mold for the incipient crystal.1a, 32, 33 In order

to understand how organisms make use of soluble additives to control crystal

morphology and transpose this knowledge to the synthesis of artificial materials,

it is necessary first to look at the composition of such biomolecules. Using

biochemical and molecular biology tools, many of such proteins have been purified

and sequenced, most notably from mollusk shells,34 bone apatite,19 and magnetite

in magnetotactic bacteria.3 Several of these proteins were used as additives during

crystal growth and provided valuable mechanistic insights into the control over

mineral formation. For example, the Mms6 protein involved from magnetotactic



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bacteria was shown to form in vitro superparamagnetic cuboidal crystals 20–30 nm

in size, while the particles synthesized without the protein were not homogeneous

in size or shape.35 – 37 This protein clearly has a role in the formation of uniform,

monodisperse magnetite crystals, and a next step would be to produce synthetic

polymers that mimic the effect of Mms6.38 For calcium carbonate, synthetic

polymers such as polyaspartic acid and polyacrylic acid, among others, have

successfully been used to tune the polymorph type and morphology of crystals.39

Most interesting is the formation of chiral morphologies in calcium carbonate

through the interaction with chiral molecules,40 and the formation of hierarchical

structures using low molecular weight and polymeric additives.41, 42

Although most biomimetic systems deal with only one or very few organic

components, when trying to mimic Nature, one must always keep in mind that

the organic matrix constituents that control the formation of biominerals generally do not function in isolation. Rather, the three-dimensional assembly of

the biomolecules into a framework is crucial for proper control over mineralization and over the properties of the material. Therefore, an understanding of the

structure–function relationship of the organic matrix–mineral composite cannot be

neglected. The importance of understanding how the matrix components function

together in mineral formation was well represented in the work of Falini et al.24

The authors assembled in vitro the major organic components of the aragonitic

nacreous layer of mollusk shells: silk, purified from the cocoon of a silk worm;

β-chitin from the pen of a squid; and acidic proteins extracted from both the aragonitic and calcitic layer of the shell. The adsorption on the silk–chitin scaffold of

proteins extracted from the calcitic layer resulted in the formation of calcite, while

adsorption of proteins extracted from the aragonitic layer resulted in the formation

of aragonite crystals. In both cases crystallization inside the chitin scaffold occurred

only when the acidic macromolecules were present. Furthermore, in the absence of

silk or when chitin was substituted by a polystyrene scaffold, the acidic proteins

from the aragonitic layer lost their ability to induce aragonite formation. While this

example deals with a structure–function relationship in terms of understanding the

formation of biominerals, this aspect is also crucial when the interest is to mimic the

properties of a biomaterial. Most notable examples are hierarchical materials such

as bone, teeth, and the skeleton of the glass sponge Euplectela.43 Their mechanical

properties, and hence their function, are highly dependent on the assembly of the

basic building blocks, from the nanometer to the macroscopic level.



6.3 APPLYING LESSONS FROM NATURE:

SYNTHESIS OF BIOMIMETIC AND BIOINSPIRED MATERIALS

So far we have discussed the major principles behind formation of biogenic

minerals in Nature, and how one can learn from the biological system. In the

present section, we discuss how we can apply what we learned from Nature to

the synthesis of bioinspired materials with tunable morphologies and properties.

Given the complexity of biominerals, it is very important to keep in mind which



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aspect of the biomaterial (i.e., morphology, mechanical, optical, or magnetic

properties) are to be reproduced, and in what length scale.

6.3.1



Biomimetic Bone Materials



Biologically inspired materials have a great potential in the fields of regenerative

medicine and biomedical engineering.44 In this case, most approaches focus on

reproducing the overall properties of the biomineral in order to restore its function in the body. One biological tissue that has been the subject of research for

biomimetic replacement materials is bone. Bone is a tissue that provides structural support for our bodies and has unique mechanical properties that arise from

its hierarchical structure and may vary according to the function that a particular

bone performs at a particular location in the body.16 Although bone is capable of

self-repair, this capability is limited to small defects and further decreases with

age and is affected by diseases. In case of severe traumas, the tissue needs to be

replaced using artificial materials in order to restore its function. Thus, there is

great interest in developing bioinspired materials that possess osteoinductive properties, being capable of inducing bone regeneration and eventually being resorbed

by the organism and replaced by bone, or that can directly be used as replacement

material.

Biogenic calcium carbonate, as found in coral skeletons and sea urchin spines,

was found to be a promising material for bone replacement and regeneration, since

it can easily be resorbed by osteoclasts and be replaced by native bone.44, 45 Furthermore, nacre was shown to have osteoconductive properties, meaning that it

stimulates the activity of osteoblasts and induces the formation of new bone. Therefore, synthetic, bioinspired organic–inorganic composites are emerging as new

materials for bone regeneration and offer more possibilities to tune biocompatibility, biodegradability, and mechanical properties.44, 46 Based on the osteoconductive

properties of biogenic calcium carbonate, synthetic calcium carbonate has been

investigated as a material with potential application in bone regeneration. Indeed,

it has been shown that thin films of crystalline CaCO3 can be used as substrates for

cell culture, being capable of supporting rat bone marrow stromal cell attachment

and differentiation into osteoblast- and osteoclast-like cells.47 These films were

prepared on a patterned block copolymer film consisting of alternating of mineralized and nonmineralized regions (Figures 6.5a and 6.5b). Furthermore, polyacrylic

acid was used to stabilize an amorphous CaCO3 precursor phase, which is important in that the amorphous material can easily be molded into any shape before

it crystallizes. Thus, it is possible to generate different patterns of CaCO3 in a

variety of substrates. While these results were obtained on two-dimensional (2D)

substrates, a follow-up investigation was performed, using the same methodology,

on three-dimensional (3D) polymer scaffolds (Figures 6.5c–e).48 The jump from a

2D to a 3D scaffold is an important step since biological tissues have a complex 3D

architecture that is crucial not only for its mechanical properties, as is the case of

bone, but also for providing spatial and organizational cues toward morphogenesis.

Bone cells are sensitive to the physical properties of their environment, such that the



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