Biomimicry

by Janine M Benyus

  To prove his point, Waite gives me a primer on primers. We prime before we paint because we hope it will help the paint stick a little better. But our primers are notoriously unreliable. Water eventually eases its way under both the paint and the primer, bubbling our house paint and spreading a rash of rust across our trusty Toyotas. Water is also the enemy in the application stage, which is why we always have to dry off a surface before we glue anything to it. That’s also why we have to dry-dock our boats to repair them, and why we have to use stitches in surgery instead of glue. We are flummoxed by the fact that crafty mussels are able to spread adhesive in the deep, cure it wet, and then count on it to stick to just about anything, all while surrounded by water. How do they do it?

  “They do it with chemistry,” says Waite, “and I became obsessed with finding out what kind of chemistry.” I look through the glass, but the byssus-building mussel “plays poker,” hiding most of what it is doing inside its fleshy foot. Waite has used molecular probes and other ingenious techniques to spy on each part of the process. As my interpreter, Waite explains what he thinks is happening inside the foot, and what we would do if we were attempting a similar feat. It’s the classic “them and us” story that biomimics are so good at telling.

  Cleaning the Surface

  “OK,” Waite says, “pretend I’m edulis.” He sticks out his arm to represent the fleshy part of the mussel’s body that protrudes from the shell, and with his hand, he begins to creep along the surface of the lab table. “The mussel uses its foot to shop around for a likely surface, and when it finds one it likes, it cleans it with squirming motions.”

  We clean surfaces too, he tells me, mainly because our adhesives really need the help. “This table might look smooth, but if you could see its molecular terrain, you’d see hills and valleys—bumps on the surface composed of positive or negative charges. If you wanted a coating of some sort—a sheet of positive charges—to stick, you’d ideally want a surface that had all its negative charges exposed. But if the surface was uneven and some of the negative charges were hidden in valleys, it wouldn’t be easy to get a bond. Because our adhesives aren’t very talented, we have to spend a lot of time preparing the perfect surface for them. A squirm here and there wouldn’t do it for us.”

  Applying the Primer

  After a rather casual cleaning, the mussel presses the tip of its foot down on the surface like a plunger to squeeze the water aside, and then deposits a mucous seal around the edges. Next, the muscles in its foot contract, lifting the ceiling of the plunger and hollowing out a bell-shaped cavity—a vacuum space. Mimicking the vacuum formation, Waite presses his palm perfectly flat on the lab table and then cups it. “Now I’m ready to manufacture a thread and disk, and attach it to the surface with an adhesive.”

  If only it were that easy for us. Before we can lay down our adhesives, Waite explains, we usually need some sort of primer that will combat water, the bad boy of bonding. Most surface molecules would rather bond with water than just about anything else. And once water grips the surface, the adhesive loses its place (which is why you can usually get a wine label off by soaking the bottle).

  A primer is designed to confound water. It occupies the chemical groups on the surface you are painting, in effect hiding the “hooks” that might get caught up in a reaction with water molecules. On glass surfaces (which love water), we prime with silanes, chemicals that imitate the bonds found in the glass itself. While one part of the silane layer occupies the glass, the outward-facing side presents chemical hooks that can bond with the adhesive, or some other polymeric material such as paint.

  But even our specialty primers are far from foolproof. If water molecules (in vapor or liquid) manage to enter through a crack or scratch, they’ll slip under the adhesive or paint and outcompete the primer, burrowing down to bond with the glass. If we had a talented enough adhesive, suggests the mussel, we wouldn’t need primers to achieve good adhesion. And we wouldn’t have to worry about our paint blistering or our cars rusting away.

  Laying the Adhesive

  In the ceiling of the bell-shaped cavity of the mussel’s foot are jets that squirt out granules: one-to two-micron-wide balls of liquid proteins that first coalesce, then harden or cure into an adhesive via the cross-linking of tangled strands of protein. In the mussel’s case, the cross-linking hooks located on the strands are doubly versatile; they cross-link to one another for cohesion (a hanging together of the glue), and they bind to the surface too, in what’s called adhesion. Conveniently, these hooks are built right into the protein.

  The other items needed for the cross-linking reaction—a chemical initiator to kick it off and a catalyst to speed it up—are also right at hand. The initiator for this chemical reaction is oxygen, which comes free for the taking in seawater. A catalyst also comes free, bundled with each mussel protein molecule. After helping to speed the cross-linking, it conveniently becomes a structural part of the glue.

  Our adhesives are woefully underequipped by comparison. We have to add not only an initiator to get things going (oxygen isn’t enough) and a catalyst to speed things up, but also a separate cross-linking chemical. That’s three steps instead of one. Despite all this effort, getting good cohesion and adhesion in one product is still a dream.

  Creating the Foamy Plaque

  Next, the mussel manufactures the solid-foam disk that anchors the end of the thread. This plaque is made of different proteins that squirt out of jets in the bell-shaped cavity. Once released, they thicken to the consistency of shaving cream and then harden into a solid foam containing air bubbles, like Styrofoam.

  “Why a holey substance?” I ask. “Wouldn’t a solid mass be sturdier?”

  Maybe, says Waite, but sturdiness is not the only thing a mussel needs. Flexibility is also a virtue. A foam will deform more easily than a solid will—allowing it to give a little. This means mussels can perch their plaques on surfaces like pilings or metal stanchions, which expand and contract over the course of a tidal cycle. Whether a mussel is baking in the sun or bathed in cold water, its plaque will give without breaking.

  Equally important, a solid foam knows when not to give. As Waite explained, “If you notch a solid substance, like glass for instance, and apply force, you’ll get a crack propagating ‘catastrophically’ as the materials scientists like to say. Use a holey material like foam, and the crack will travel only to the first void and then lose steam. It’s called a crack-stopping strategy. In wood, the voids are those longitudinal tubes where the sap travels. When you cut a log across the grain you keep hitting them—that’s why you stand logs on end in order to split them.”

  When we make a solid with holes—Styrofoam, for instance—we use what’s called a blowing agent to force bubbles into a vat of thickening polymers, or plastic. Unfortunately, the blowing agents of choice are CFCs (chlorofluorocarbons), which, when released to the air, react with the atmosphere and tear up the ozone layer. In light of the hole gnawed in the atmosphere above Antarctica, global leaders have begun to call for bans on the production and use of CFCs. The first phaseout in this country started in 1996, as specified by the Montreal Protocol on Substances that Deplete the Ozone Layer and the 1989 revisions to the Clean Air Act.

  With the CFC ban on the horizon, industry was anxious to find a way to make Styrofoam without ozone-depleting chemicals. The military was especially motivated, since it regularly tests explosives against thirty-foot-thick sheets of the stuff. One major consumer, the Picattiny Arsenal in New Jersey, spearheaded research into a CFC-free process.

  Its elegant solution answered a question that Waite had been struggling with. “What I couldn’t figure out was how the mussel could produce a solid foam without using a blowing agent. When I read about the new gas-free process, I said, of course, this is how mussels must do it! Here we are, toasting the inventors of the new Styrofoam at award ceremonies, not realizing that mussels have been quietly doing the same thing for millions of years.”

  The
old way of making Styrofoam is to pour styrene molecules into organic solvent and wait for them to link into polymer chains thousands of monomers long. As the chain grows, the solution becomes thicker and thicker, eventually turning the consistency of peanut butter and then peanut brittle. Somewhere in between, you blow in a gas to form air spaces—which in technical lingo is called “injecting a gas phase into a liquid phase.” No other gas works quite as well as CFCs.

  Finally, someone working on the problem thought: Instead of injecting a gas phase, why don’t we put a liquid phase into the liquid phase—like oil into water—and have one liquid evaporate while the other solidifies? The big problem was that styrene molecules are just like oil—they hate water and tend to simply settle out in clumps at the bottom of a beaker long before the water evaporates.

  The chemists working on this problem should have just taken a break and gone to the biggest salad bar in town. As it turns out, the riddle of keeping an oily liquid suspended in water has a simple solution, one that we benefit from every time we dress our radicchio. Colloidal chemists call it the “salad dressing model.”

  In prepared dressings, food manufacturers add egg whites to form an emulsion that keeps oil droplets distributed throughout the vinegar so you don’t have to keep shaking the bottle. This process works because egg-white proteins are molecules with water-loving heads and fatty, water-fearing tails. To get away from water, the fatty tails all point toward oil droplets, while the water-loving heads stick out into the vinegar. You wind up with separate oil droplets, each surrounded by a skin of egg-white molecules. Carried by these emissaries, the oil droplets stay suspended.

  Instead of using egg whites to escort the styrene monomers, the new-Styrofoam researchers used detergent molecules, which are also schizophrenic when it comes to water. Their fatty tails circle around a small group of styrene monomers, forming a “micelle”—a tiny reaction vessel with styrene inside. Literally thousands of these detergent micelles begin to form in the beaker. Inside each one, the styrene monomers begin linking up into a chain. When neighboring micelles collide, the thickening substance from one micelle breaks through its detergent wall and forms a bridge to the growing chain in the next micelle. This happens repeatedly until all the micelles are connected in a giant, solidifying meshwork. Before you know it, the tables have turned, and the water that once surrounded the styrenes is now trapped inside their slowly stiffening lattice. As the folks from Picatinny found out, you can pick up the solid lattice, put it on a drying block to wick out all the water, and voilà!, you have air inside a solid, sans CFCs!

  In technical lingo, this is called a phase inversion. Styrene inside water becomes water inside polystyrene. Waite’s theory is that the same phase inversion happens in the mussel’s bell jar. The plaque proteins drop into water, and as they cure, the water becomes trapped inside their thickening cross-links. When the water drains out, the mussel has a solid foam plaque containing air bubbles, which is then wrapped in sealant.

  I wonder aloud how many other things the lowly mussel had beaten us to, and what we could learn that was new. “We haven’t even gotten to the byssus thread,” says Waite with a brief smile. He can see me getting hooked on edulis, and it pleases him. In his understated way, he is absolutely on fire talking about this bivalve. The lab has long ago emptied out and the lights in the parking lots have flickered on, and neither one of us has budged for hours.

  Self-assembling the Thread

  The thread is the translucent protein fiber that connects the mussel’s soft body to the foamy plaque. “To form the thread,” explains Waite, “the entire foot body forms a longitudinal groove, curling in on itself the way some people can curl their tongues. The outer edges of the groove seal and the muscles in the foot balloon out to create a negative space in the groove, a vacuum. Numerous jets along the body of the foot squirt out granules of thread protein, each jet secreting a slightly different variation of protein, custom-mixed to perfection. These proteins are massaged into place by muscles and then left to self-assemble and cross-link.”

  When we produce fibers from cross-linked polymer, we, too, use jets to shoot the raw material into a chamber. We do what’s called extrusion—a large-diameter screw turns inside the chamber, spiraling the precursor material slowly forward toward a die. The die imposes some sort of ordering or shape as the fiber is extruded, in the same way that a pasta machine makes fettuccine or rigatoni. The difference between us and the mussel is that our fibers are monolithic in character: chains with little or no variety in their subunits, uniform throughout.

  The byssus, on the other hand, has a multiple personality. When Waite analyzed the thread, he found that it is made of hundreds of protein molecules, all slightly different in composition. Though their core is collagen protein, like our tendons, each molecule has a portion that is either springy, like natural rubber, or rigid, like natural silk. The proportion of springiness to stiffness depends on where in the thread the protein is located. The molecules at the mollusk end of the thread are springier, while those near the plaque are stiffer, presumably to give the thread the soft-and-hard qualities that it would need in its turbulent home. In testing, Waite found that this customizing of the proteins makes byssus a lot stiffer, tougher, and more elastic than pure collagen would be.

  The gradient from the springy top of the thread to the stiff end is not abrupt, however; there is no interface or line drawn between the two. As Paul Calvert had told me, nature loathes fasteners—instead it blends gradients so that the fiber has no single vulnerable point. Waite speculates that such a bifunctional thread would be something we could use for prostheses, or even for robot tendons. The elbow portion of a robot arm could incorporate the rubbery segments, he suggests, while the forearm and upper-arm parts could have stiffer natures. And coating it all, says Waite, could be an edulis-inspired sealant that would be even more amazing.

  Sealing the Thread

  “To me, the transparent sealant that coats and protects the byssus is one of its most exciting features,” says Waite. “Byssus is food, after all—it’s protein. The only thing that keeps it from being eaten immediately by the voracious microbes in the sea is its sealant.”

  After the thread and plaque are formed, the whole structure gets coated with yet another set of protein granules that coalesce, spread out evenly, and set to a lacquerlike finish. (The process here is uncannily like the one we use to coat tiny time capsules.) For its finale, the mussel secretes a releasant over everything—a mucuslike substance that allows the newly cast thread and plaque to separate from its mold. Like a curator uncovering a brand-new painting, the mussel removes its foot and the sealed byssus sparkles in the sea light. Although the sealant is itself made of protein, its structure makes it impervious to microbes, at least at first.

  “What’s neat about the sealant is that it doesn’t stay permanently impervious to microbes. The mussel may use its byssus for a few hours or a few days. When it’s time to move on, it leaves its byssus behind. In two or three years, the sealant falls apart and the microbes get to feast.

  “The reason that excites me,” says Waite, “is that we have a lot of consumer products that we use briefly and then throw away.” He goes into a lab drawer and pulls out a box of hundreds of pipette tips. He pours them on the slate top and they scatter. “Petrochemically derived plastics like this will virtually last forever in a landfill. Our greatest sin is this overengineering—we may not be able to live forever, but we make darn sure that our waste will.”

  Waite’s idea is to make disposable things that will last only as long as we need them. “We could use natural materials like collagen, silk, rubber, cellulose, or chitin [from crab shells] to produce fibers or containers or whatever, and then seal them with the mussel-type sealant. After two or three years, the sealant breaks down and microbes in the landfill invade the degradable material underneath. Back it goes, into the food chain.

  “When you take a natural polymer and coat it with a natural polymer t
hat degrades much more slowly, then you’re going toward ideal design that doesn’t fly in the face of modern technology. We can still have some throwaway items, but instead of burying or burning them, we can compost them. The degradation can be put off, but not indefinitely the way it is now.”

  No wonder Waite wants someone to make edulis a superhero. The patents in this one seemingly ordinary animal would support a whole industry. One reason it may have taken innovators so long to look at edulis was suggested to me by Randy Lewis, a silk researcher at the University of Wyoming. “Natural materials are difficult to interrogate,” he told me. “They’re often insoluble proteins, meaning it’s tough to get them to separate out. They’re usually huge molecules, and until very recently, we haven’t had the tools to visualize them. Some of the most interesting are composed of highly repetitive sequences, which, once they are broken into pieces, are like a jigsaw puzzle with only one color—hard to put back together again. As a result, even if funding agencies agree that silk or bioadhesive is an interesting material, they’re not certain you’ll be able to get to the bottom of it. They usually fund something else that’s a surer bet.”

  Herb Waite has been trying to get to the bottom of a natural material for longer than most. When I ask him how many of the byssus proteins he has left to characterize, he is cagey. “Well, so far we’ve characterized four proteins called Mytilus edulis foot protein or MEFP1 through 4. MEFP1 is the sealant, MEFP2 is the structural molecule in foam, MEFP3 looks like it’s present at the foam interface, but that may be a limitation of our technique. I don’t know what MEFP4 is yet. We’ve also got two collagens from the thread, three DOPA-containing proteins [DOPA is 3,4-dihydroxyphenylalanine], and one enzyme. I have to do another DOPA-containing protein and as many as ten minor proteins and an enzyme.” Suddenly he stops counting and waves it all away. “I don’t really concentrate on how many I have left. It’s like climbing a mountain—you don’t want to look up and see how far you have to go; it doesn’t help. The only thing that helps is to put one foot in front of the other.