Biomimicry

by Janine M Benyus

  Life-friendly manufacturing processes

  An ordered hierarchy of structures

  Self-assembly

  Templating of crystals with proteins

  Each of the tricks was new to me, and probably new to many of the other conference attendees who kept stopping by out of curiosity. What sets the biomimics apart from their peers is that nature’s canon has become their own. If the biomimics had their way, these lessons would be the backbone of every materials engineer’s education. For the purposes of this chapter, we’ll take the short course.

  HEAT, BEAT, AND TREAT

  In the hive of the MRS meeting, forty mini-meetings called symposia are held concurrently. In each one, new findings are introduced in papers given every fifteen minutes, all week long. Most of the talks focus on the new alchemy: the synthesis of new alloys, new ceramics, new plastics made possible by impossibly high temperatures, high pressures, and strong chemical treatments. “Heat, beat, and treat” has become the de facto slogan of our industrial age; it is the way we synthesize just about everything.

  Nature, on the other hand, cannot afford to follow this strategy. Life can’t put its factory on the edge of town; it has to live where it works. As a result, nature’s first trick of the trade is that nature manufactures its materials under life-friendly conditions—in water, at room temperature, without harsh chemicals or high pressures.

  Despite what we would call “limits,” nature manages to craft materials of a complexity and a functionality that we can only envy. The inner shell of a sea creature called an abalone is twice as tough as our high-tech ceramics. Spider silk, ounce for ounce, is five times stronger than steel. Mussel adhesive works underwater and sticks to anything, even without a primer. Rhino horn manages to repair itself, though it contains no living cells. Bone, wood, skin, tusks, antlers, and heart muscle—miracle materials all—are made to live out their useful life and then to fade back, to be reabsorbed by another kind of life through the grand cycle of death and renewal.

  It was fun to watch the milling scientists from other disciplines stick their heads into the doorway of Symposium S. While most rooms at a meeting like this are resplendent with the talk of unearthly synthetics, Symposium S featured slides of coral reefs and tall trees, spruce bogs and spiderwebs brushed with dew. The latest high-tech materials here weren’t experimental designs—they were ancient, biological inventions, tested and proven over millions of years on Earth. The same Earth on which we and our materials are trying to survive.

  The people in Symposium S have little allegiance to the heat, beat, and treat mantra. They see the handwriting writ large—the dwindling oil reserves, the toxic nightmares of our own making, the high failure rates (breaking, cracking, stretching out of shape) of many of our materials. Despite our colossal energy expenditures, we still can’t make materials as finely crafted, as durable, or as environmentally sensible as those of nature. The rhinos, mussels, and spiders in the slides all seemed to be wearing Mona Lisa smiles. Somehow, out of the world’s most common chemicals, like carbon, calcium, water, and phosphate, they fashion the world’s most complex materials. As any biomimic in the room could tell you, the S in Symposium S stands for surprise.

  THE HARD STUFF FIRST

  The papers presented that week split along two lines, the mostly inorganic (the hard) and the mostly organic (the soft). Nature’s inorganic materials are tough, used for skeletal structure or protective armor, the shells and bones and spines and teeth of the natural world. They are crystallized versions of Earth-derived materials—chalk and phosphates, manganese and silica, even some iron thrown in for “bite.” Since organisms don’t produce these inorganic minerals in their own bodies, they must find a way to tempt and tame the particles of the Earth to settle and crystallize in just the right location. If you’re a soft-bodied mollusk living in the rock-and-roll of the tidal zone, for instance, the best place to have a shell crystallize would be right over your head.

  Oyster Envy

  Rich Humbert owns a wetsuit that doesn’t quite keep him warm. Even with a neoprene mask strapped over his bearded face, he must let his eyes show, and by the time he bursts up for air, his robber’s mask of exposed skin is a painful shade of purple. All of which makes diving for abalones in Washington’s San Juan Islands a lonely vocation.

  “Most people prefer to encounter their abalones in souvenir shops,” he tells me. “But I like to get in with them, see where they live.” He pantomimes the hunt for me. “You reach down for them through the murky tidal wash, feeling with your hands. The outer shell is drab and scabby with barnacles. It’s hard to believe that inside there’s this smooth, luminous, mother-of-pearl lining. The idea is to grab them as soon as you touch them, before they can suction themselves to the rock.”

  A tickled abalone can be wickedly fast. So powerful is its foot suction that if you miss the magic moment, you have to pry it from the rock with a tire iron. For abalone aficionados like Humbert, a pry job is the sign of a hacker, and he would rather turn completely purple than resort to one.

  Most people who hunt abalone eat the meat and sell the shell, but Humbert dives and plucks for what he can learn. He’s part of the University of Washington’s team investigating abalone nacre, the smooth inner coating that is delicately swirled with color and, best of all if you’re a ceramist, hard as nails. “Ever try jumping on an abalone shell?” asks Humbert. “A car could drive over these guys and not faze them.” Back at the lab, he has to fire up industrial machinery to break the outer shell and nacre into pieces. One shell—a beautiful eight-inch platter—will be enough to last through a year of research.

  To the naked eye, the piece of nacre that Humbert hands me looks smooth and featureless. Then he shows me an electron-microscope picture of the same piece in cross section. Standing out in bold, black-and-white relief is the intricate crystal architecture that accounts for the shell’s ability to shrug off stress. Looking in from the side, you see hexagonal disks of calcium carbonate (chalk) stacked in a brick-wall motif.

  If you look closely between the bricks, you can see a narrow mortar of squishy polymer. The polymer acts like a thin smear of chewing gum—it stretches ligamentlike when the disks are pulled apart and it slides and oozes in response to head-on stress. If a crack does get started, the brick-wall pattern forces the crack to follow a tortuous path, stopping it in its tracks. As a result, “Abalone is twice as tough as any ceramic we know of—instead of breaking like a manmade ceramic, the shell deforms under stress and behaves like a metal,” says Mehmet Sarikaya, whose name appears in the credit line for many beautiful electron-microscope pictures of abalone.

  Portraits of the nacre taken from above show a further complexity. On any one level of the brick wall, the hexagonal disks are twinned: Their shapes and placement echo one another, as if a mirror is between them. Individual disks are composed of twinned “domains” that also mirror one another. Even the grains within each domain are twinned, showing the mathematical repetition and beauty that characterize natural form.

  Closer to home, a soft material in our own bodies has become the poster tissue for this concept of repetition at many scales. The “unraveled tendon” drawing (which got a lot of screen time at the meeting) shows a hierarchy that is almost unbelievable in its multileveled precision. The tendon in your forearm is a twisted bundle of cables, like the cables used in a suspension bridge. Each individual cable is itself a twisted bundle of thinner cables. Each of these thinner cables is itself a twisted bundle of molecules, which are, of course, twisted, helical bundles of atoms. Again and again a mathematical beauty unfolds, a self-referential, fractal kaleidoscope of engineering brilliance.

  In the human tendon, in the abalone shell, in the stacked plywoodlike layers of the rat’s tooth—over and over again at the meeting, this issue of “structure granting function” came to the fore. The multileveled complexity of these materials is referred to as an ordered hierarchical structure, which seems to be nature’s second trick of the
trade. From the atomic level all the way to the macroscopic, precision is built in, and strength and flexibility follow.

  But how does nature manage to create that microstructure? And how can we do the same? Answering those questions is at the very heart of what biomimics are trying to do. “We want to do more than just copy down the angles and the architectures of nature’s designs or build our materials in their image,” says ceramist Paul Calvert from the University of Arizona Materials Laboratory in Tucson. “What we really want to do is imitate the manufacturing process, that is, how organisms manage to grow, for instance, perfect crystals and form them into structures that work.”

  All of the materials scientists I talked to agreed with Calvert’s assessment. They were itching to grow lattices with dress-parade perfection, to control crystal size, shape, orientation, and location, especially in the world of ceramics.

  The ceramics we’re most familiar with are glass, porcelain, concrete, mortar, bricks, and plaster, but as Paul Calvert says, “Ceramics have gone far beyond toilet fixtures and cereal bowls.” They are now being used in all kinds of high-tech applications—as insulators, guides, bearings, wear-and temperature-resistant coatings, and in devices that need certain optical, electrical, and even chemical characteristics, such as sensitivity to gases or the ability to accelerate a chemical reaction. For all we are asking ceramics to do, it’s ironic that we’re still using Stone Age techniques to manufacture them. Basically, we take earthy inorganic particles and subject them to heat or pressure in order to squeeze them together into a substance that is hard. Says Calvert: “Our biggest problem is cracking—brittleness. In recent years, we’ve been making incremental progress by making our grains finer and finer. We finally have them down to the nanometer size, but we’re still plagued by brittleness.”

  A few years ago, Calvert thought it was time to energize imaginations, so he and other biomimics began to look at natural designs. They uncovered plenty of examples of biological organisms that, like the abalone, sport hard body parts made from a mixture of inorganic minerals and organic polymers. Your bones are crystals of calcium phosphate deposited in a polymer matrix, for instance. Diatoms—those microscopic sea creatures that look like living snowflakes—have skeletons made of silica glass shaped by the organic membranes of their bodies. Teeth are inorganic crystals, as are sea-urchin spines and snail shells. The ultrahard crystals in a lamprey’s “teeth” are what allow it to rasp through rock. Nature is even able to utilize some magnetic material in its mineralizing process. For instance, a bacterium that was discovered in the late seventies grows crystals of iron oxide—magnetite—in tiny vesicles (balloons) inside its body. These magnetite-filled vesicles line up like beads in a key chain, and together they help the bacteria orient down toward the magnetic center of the Earth, which is also toward the anaerobic zone where they find their food.

  In all these cases, nature’s crystals are finer, more densely packed, more intricately structured and better suited to their tasks than our ceramics and metals are suited to ours. The biomimics decided it was time to find out why.

  Pearls of Wisdom

  To understand how organisms manage this trick, it helps to understand the softer side of the composite mix. For this we have to go to the molecular level—a level smaller than Sarikaya’s electron microscope can reveal. “That thin smear of polymer is more than just mortar sticking the bricks together,” says Rich Humbert. “It’s made of polysaccharides (sugars, essentially) and proteins, and they’re the ones actually running the show.” In fact, when an abalone “decides” to build nacre, the polymer mortar is erected first, and then the bricks.

  This counterintuitive ordering occurs in a similar way in many biomineralizing organisms. First the organism’s cells secrete proteins, polysaccharides, or lipids (depending on the species) into the fluid surrounding them. These “framework” polymers self-assemble into three-dimensional compartments (cubes, rectangles, spheres, or tubes) defining the space that is to be mineralized. “You can think of the framework polymers as the walls and ceilings and floors of a room that will eventually be infilled with mineral crystals,” says Humbert. In the case of the abalone, the organism builds not just one room but an entire apartment building, laying down one story of rooms after another, each slightly offset from the one below to accomplish the interlocking brick-wall motif.

  Inside each room is seawater saturated with calcium ions and carbonate ions—charged particles that will eventually land and aggregate into a crystal of calcium carbonate (chalk). Because the ions are charged, they don’t just randomly precipitate out of solution—they are attracted to oppositely charged chemical groups protruding from the walls of the rooms. Once that first layer of ions settles out, it sets the tone for the rest of the crystal. Like the bits of dust in the supercooled beaker of your high school chemistry lab, the first ions will act as seed kernels or nucleators, and the rest of the ions will settle around them, growing a crystal of a particular shape. Since the crystal’s strength and function depend on shape, the ions’ landing locations turn out to be key.

  The mollusk, evolutionarily eager to build a shell of herculean strength, found an ingenious way to get those ions to settle into a particularly strong shape. Here’s how it works: After the framework of rooms is assembled, the mollusk releases templating proteins into the inner rooms. These proteins self-assemble into a “wallpaper” that peppers the room with an orderly array of negatively charged landing sites. If we were the size of atoms, we could walk among the chemical groups and feel their electrostatic pull, beckoning to positively charged ions in the seawater, such as calcium.

  To visualize the proteins in this special wallpaper, a quick biology lesson is in order. Proteins (which make up 50 percent of the dry weight of every living cell) are large 3-D molecules that begin as long necklaces of dozens or even hundreds of chemical groups called amino acids. Each amino acid has a different constellation of charges, and when the chain is released into the fluid of the cell, those charges cause the protein to fold up in a very particular way.

  The folding pattern has a lot to do with how the amino acids take to water. Neutral, water-fearing amino acids will burrow into the center of the protein complex, while the charged, water-loving ones will take to the periphery. The amino acids also interact with one another—some repelling their neighbors and straining to get away, others meeting in a bond. What results is a three-dimensional shape, a form uniquely suited to its function. A protein may have a structural role in the body, assembling into tissues and skeletons, or it may have a “trade.” Hemoglobin, insulin, neuron receptors, antibodies, and enzymes (which orchestrate and speed up chemical reactions) are all proteins, plying a particular trade based on their shape.

  In the case of the templating proteins of abalone, the protein chain folds into a zigzag shape which bonds side by side with other zigzagging proteins to form an accordion-pleated sheet (the wallpaper). There are two “faces” to this sheet—some groups of amino acids stick out into the room, while others are embedded in the walls, floor, and ceiling like anchors. Daniel Morse, director of the Marine Biotechnology Center at the University of California in Santa Barbara, has determined that the groups that anchor in the walls are neutral (principally glycine and alanine) and those that stick out into the room are negatively charged (principally aspartate).

  The landing sites on the pleats are not random, either. Because each zigzag protein is itself precisely formed (templated by DNA), its amino acids are studded along its surface predictably. Every few nanometers, they sit ready to snag oppositely charged ions floating by in solution.

  How the ions are arrayed in that first layer says everything about how the crystal will look and function. One pattern may yield rhombohedral crystals like those in nacre; another will yield prismatic crystals like those in the abalone’s hard outer shell. Different shapes and orientations and sizes determine whether the crystal will have optical qualities, be able to conduct electricity, or be hard or soft
. There are fourteen different shapes of crystal that are possible in all of nature.

  Now, what if we were able to template for any one of those fourteen kinds of crystals by using different protein craftsmen? What if we could coat an object with a film of proteins and then dip it in seawater and have nacre self-assemble into a hard coat? That’s the dream, and there’s one fact that makes it possible—proteins don’t need to be in a living cell to do their thing.

  A protein separated from a living cell is still a protein—fully charged and able to direct crystallization. In fact, that’s what happens in the abalone—the proteins are pumped outside the cells into a seawater-filled gap between the soft body and the harder outer shell. That means, theoretically, that we should be able to fill a beaker with proteins and seawater and watch as the proteins self-assemble into their rooms and their wallpaper and the ions nucleate and begin to grow into crystals.

  Self-assembly, then, is nature’s third trick of the materials trade. Whereas we spend a lot of energy building things from the top down—taking bulk materials and carving them into shape—nature does the opposite. It grows its materials from the ground up, not by building but by self-assembling.

  Self-assembly rides the riot of forces ruled by classical and quantum physics. Like charges repel like charges, but opposites attract. Weak electrostatic bonds hold molecules together gingerly, and as conditions change, they can easily correct and adapt. Stronger, more permanent bonds are consummated with the help of lock-and-key catalysts called enzymes.

  Before any kind of bond can be formed, however, wandering molecules must first collide, like guests at a cocktail party. The energy that keeps molecules mingling comes from what scientists call Brownian motion, named after Robert Brown, an early-nineteenth-century botanist who asked the world, “Have you ever noticed that pollen grains stay suspended in water all by themselves?” (In those days, an observation like that could make you famous.) A generation later, Albert Einstein explained that the pollen grains are buoyed by the fact that invisible water molecules are continually knocking into and moving them. This restless bumper-car action of molecules also occurs in air, which is why dust particles look as if they’re dancing in sunbeams.