Biomimicry

by Janine M Benyus

  Biochemist Thomas A. Moore, a leprechaunish baby boomer who tries his best to be a curmudgeon, is frowning at his computer screen when I walk in. Epithets in a soft Texas accent. As if in response, his Macintosh lets out with a guitar riff: “That’ll be the day/when you say good-bye-yie-yie/ that’ll be the day…” On his growl, it backs down.

  “It’s telling me to get to work,” he stage-whispers, “but we’ll ignore it.”

  This seems to please him. Tom Moore is the kind of person who rubs his hands together when he’s about to dive into something—a debate, a good meal, a prickly scientific question. There’s a certain gusto with which he tears off pieces of life and chews them up. When I ask him to explain photosynthesis, he visibly brightens and (after how many years of teaching?) literally leaps up to the white board and starts drawing. “It’s amazing,” he tells me. “Being able to mimic even a small part of this process reassures me—I say to myself, see?, this isn’t magic.”

  Magic or not, mimicry doesn’t diminish the wonder that Moore obviously feels. Every now and then, in between bursts of impassioned sketching—formulas, cells, bacteria, leaves—he says, “I have to go soon.” Instead, the clock hands spin, and I learn how the sun turns light into life.

  ELECTRON PINBALL

  Moore tells me that sunlight is like a drizzle of energy particles, and the job of each green plant, blue-green alga, and photosynthetic bacterium is to capture those particles and put them to work. To help increase their odds, these photon harvesters spread out an array of light-sensitive pigments—chlorophyll a, chlorophyll b, and carotenoids—that act like antennas for the sun’s energy. The atoms in each pigment are arranged in the shape of a lollipop—a ring atop a stem. Hundreds of lollipops are embedded in the skin (membrane) of a fluid-filled sac called a thylakoid. Hundreds of thylakoids are stacked up like water balloons inside each chloroplast. Chloroplasts, which make a green plant green, are packed by the hundreds of thousands, if not millions, in even the tiniest leaf.

  When sunlight hits these chloroplasts, the lollipop antennas in the skin of the thylakoids grab the packet of energy, then funnel it down to one of the “photosynthetic reaction centers,” also embedded in the thylakoid’s skin. Each reaction center is a sprawling, ten-thousand-atom assembly with its own set of two hundred lollipop antennas. At its heart is a pair of two highly sensitive pigment molecules that do the actual absorbing. Label this Photosynthesis Central, where light becomes food for life.

  Now come in for the close-up. Zooming around this chlorophyll—around all molecules, for that matter—are electrons in orbit, just like the ones you see in those 1950s logos for Atomic cleaning detergent. These electrons are negatively charged particles, the very same ones that, when they cooperate in a flow or current, will toast your English muffins for you. To picture photosynthesis, you have to keep your mind’s eye on this moving cloud of electrons. When a leaf absorbs the energy of the sun, some of those electrons zooming around the chlorophyll pair get so excited that they start to migrate to other molecules, setting off a chain reaction in which water is split, oxygen is freed, and carbon dioxide is turned into sugar. In a leaf like the duckweed, it takes two different kinds of photosystems (PS I and PS II) to accomplish this solar alchemy.

  Each photosystem stakes out its own portion of the light spectrum. Photosystem II, for instance, absorbs wavelengths that are 680 nanometers long (reddish light), and this absorption causes one of the electrons circling the central chlorophylls to hop to a higher energy orbital, like a pinball being sprung into play. Before it can relax back to its old orbital, discharging its energy as useless heat, an “acceptor” molecule stationed nearby snatches the electron away. But right next door to the acceptor, there’s another molecule that’s an even better acceptor, and zap!, it steals the electron. The electron continues traveling like a hot potato, tossed molecule to molecule away from the chlorophyll. In a few hundred trillionths of a second, a negative charge winds up at one end of a chain of acceptor and donor molecules, and a positive charge winds up at the other. The positive charge is actually a “hole” on the central chlorophyll, created when the electron was whisked away.

  Since nature abhors this sort of hole, a nearby molecule code-named Z donates an electron and resets the chlorophyll, sort of like a pinball machine reloading with a new ball. Soon it’s off to the races again, with another energetic photon of light captured and a new electron being sprung out of its orbital and into play.

  In the meantime, the first hot-potato electron that has been traveling from acceptor to acceptor now jumps the pinball table entirely and goes to the other photosystem, PS I. There it meets a central chlorophyll that has recently absorbed a photon of light (700-nanometer wavelengths) and sprung its own electron into play. That leaves it with a hole, which is conveniently reset by the electron hopping over from PS II. Again, there is a hot-potato toss in PS I as the electron moves from one acceptor molecule to another. The electron eventually moves to the outside of the thylakoid membrane, while the positive charge (all the way back at particle Z in PS II) remains close to the inside of the membrane.

  At this point, Moore wheels around and points his marker at me. “And what do you have when you have a positive charge on one side of a membrane and a negative charge on the other?” He’s like a demented game show host. I have no idea. “MEMBRANE POTENTIAL!” he shouts, as if we’ve hit Double Jeopardy.

  Every now and then, you discover a scientist’s true fetish, the concept that absolutely floors them. Given the chance to explain it to the uninitiated, they stop flatfooted for a moment. There is so much crowding at the door waiting to get out—how will they begin?

  “The difference,” he goes slowly, patiently, “between a dead bacterium and a live one is membrane potential. In living cells, the concentration of chemicals or charges inside the enclosing membrane is different from the concentration outside. The law of entropy says that all systems want to go to a position of lower energy—they want to equalize uneven gradients or concentrations. That’s why a spot of ink breaks up in water—the concentrated ink molecules diffuse into the water and the water molecules diffuse into the ink. Once the concentrations are equal, the system can relax.

  “A process like photosynthesis actually creates unequal gradients. It moves negative charges to the outside of the thylakoid membrane, leaving a buildup of positively charged ions inside. This polarizes the membrane, making the inside of the sac different from the outside. The charges on either side of the membrane want to recombine, to release their energy and relax; that would be a downhill reaction, the most natural thing in the world. But because the membrane is in the way, the tension remains high. Your car battery does the same thing—it separates charges as a way of storing energy. Living cells, like cars, can use that energy potential. They use it to import nutrients, to get neurons to spark, to get cells to talk to one another, or to get muscles to move. On a cellular level, life lives in the tension between unequal concentrations, unequal charges. Membrane potential equals chemical and electrical potential equals life.”

  At this point, having not cracked a cellular biology textbook for many years, I felt the concept wobble out of my reach a little. Moore, the consummate teacher, returned to the leaf.

  Membrane potential has a lot to accomplish in plants, namely the feeding and fueling of an entire planet. First, there’s the splitting of water. With each electron that the PS II chlorophyll springs into play, the molecule Z donates one of its electrons to “reset” chlorophyll. Z eventually donates four electrons to PS II. To reset its positive holes, it teams up with a water-splitting complex that strips four electrons from water (H2O). This liberates oxygen, which percolates out of the leaf, and hydrogen ions (H+), which get stuck inside the thylakoid sac. Hydrogen ions, being positively charged, want desperately to even the score and get to the outside where negative charges reside.

  In the meantime, at the outside of the membrane, one shuttled electron after another is handed off to a mol
ecule called NADP+ (nicotinamide adenine dinucleotide phosphate). This hand-off transforms NADP+ into the electron carrier NADPH, which has mighty “reducing” powers (the ability to give electrons to other compounds). This means that in the next stage of photosynthesis, the so-called dark phase, NADPH can give electrons to CO2, and thus “reduce” it to sugar, CH2O. But it can’t do that without a sidekick—a molecule that will provide energy.

  “And here,” says Moore, “is where the membrane potential comes in.”

  The only way for the trapped hydrogen ions to get out of the thylakoid sac is through an enzyme “channel” called a coupling factor. In textbook cartoons, it looks like a toadstool, with a stem spanning the membrane and a bulbous head sticking outside. As the plus charges escape through this coupling factor, they extract a toll—they turn a compound called adenosine diphosphate (ADP) into adenosine triphosphate (ATP) by adding a third phosphate. This third phosphate is hitched to the other two with a high-energy bond, and it is here that the energy of the sun is stored. During the dark reactions, ATP’s high-energy bond is severed and the energy is used to turn CO2 into sugar.

  The chemistry that stored this energy couldn’t have occurred without two charges, a plus and a minus, being banished to opposite ends of a membrane, sent packing by the power of ordinary, garden-variety sunlight. Anytime you have a positive and negative charge separated like that, you essentially have a battery, a battery powered by the sun.

  Moore takes another deep breath. “We began to wonder if we could make a solar battery by hooking a sun-sensitive pigment to a string of donor and acceptor molecules. We wanted two things. First, we wanted to get charge separation—a plus at one end of the string and a minus at the other—and second, we wanted the charges to stay separated long enough for us to accomplish work.”

  “Work” could take many forms: 1) Hook wires to the ends of the molecular string to get an electric current, 2) use it to split water and produce clean-burning hydrogen gas, 3) use it as a power pack to drive solar-based manufacturing, or even 4) use it as a switch for computing near the speed of light.

  “One day, we may even convince our string of molecules to go into the membrane of an artificial cell,” says Moore. “Instead of boiling chemicals for several hours in toxic solutions to make plastics or other products, you could build a tiny reaction vessel, give it a power pack, and stand back so you’re not blocking its sun.” What’s science fiction for us—clean-burning fuel and chemistry in sunlight—is commonplace for plants. Somebody needs to tell Aristotle that the gods are in the kitchen after all.

  SOLAR ALCHEMY

  Speculation is a lovely sport, but as any of the scientists at the center will tell you, it’s one thing to work out a prototype of a donor-pigment-acceptor device on paper. It’s quite another animal to actually hook the molecules together so they’ll transfer electrons. Putting theory into practice means taking small steps into uncharted (by humans at least) terrain, working from maps that are sketchy at best. But considering the fact that photosynthesis produces 300 billion tons of sugar a year, it is undoubtedly the world’s most massive chemical operation. Every pine needle and palm leaf can do it. The more I thought about it, the more amazed I was that no one had taken Ciamician up on his dare. How hard could it be to duplicate the first few picoseconds, the electron transfer part? And why haven’t we done this before?

  That was before I saw the molecular map of a photosynthetic reaction center. Devens Gust has a full-color reproduction of a purple bacterium’s reaction center in his office, and he and I spent a while just admiring it. The visual was relatively new to those who had been studying photosynthesis for years. As Gust examines it, his black eyes focus like a hawk’s on a gopher hole, and for a moment, I lose him.

  Devens Gust is a deep river of a man, possessing a trademark calm that plays well in combination with Tom Moore’s quick passion. While Tom and his research partner Ana (who is also his wife) are usually in the office long after the dinner hour, Gust closes his door at five and rarely shows up at the lab on weekends. “Devens can get more done in a forty-hour week than most of us get done in seventy,” Tom Moore tells me. Before I left, Gust pulled out a map and helped me plan a road trip across Arizona, showing me where I could find Anasazi ruins that the tourists pass by. “That sounds like Devens,” said Moore. “He actually has time to go hiking!” And time enough, with a deadline looming, to show me the heart of what inspires his team.

  The reaction center is a startlingly beautiful device, composed of several chemical groups called cofactors, set like jewels in a tangled bird’s nest of protein—what scientists call the protein pocket. When you connect the cofactor dots, you get something that looks like a wishbone, with a chlorophyll pair in the center and two curving bones of cofactors facing one another with near mirror symmetry. Ten thousand atoms are choreographed in the membrane just so, with a geometry that allows them to play the pinball game of electron transfer. Faced with a blueprint this complex, what steps would one take to build a solar battery from scratch?

  “We knew it would be ludicrous to try to duplicate anything as complex and finely evolved as this,” says Gust. “Nature has a three-billion-year jump on us here.” The purple bacterium we are admiring is a sun-harvesting microbe that researchers routinely study for clues to photosynthesis. It’s sort of the fruit fly or E. coli of photosynthesis research because it’s easy to culture, easy to read genetically, and structurally simpler than green plants. It’s more akin, they believe, to the first photosynthesizers that arose three billion years ago. Instead of two photosystems, purple bacteria make do with one that is analogous to PS II. “Because people have been studying the purple bacterium so intensively, its reaction center has fewer black boxes than any other system; it’s the closest thing to a blueprint that our team has.

  “Our goal was to pare down the reaction center and model only its essence. We wanted our device to work like this, even though we knew it would not look at all like this.” The natural reaction center, for instance, uses that tangled scaffolding of proteins to embed and hold independent cofactors. Not wanting to tackle anything as complex as a protein pocket, the team took a different route. In their device, the cofactors float in a beaker of liquid, bonded to one another with great care via organic chemistry techniques.

  “The bonds must duplicate the scaffolding’s magic—they have to hold the molecules at the correct geometry and distance from one another to provide the proper pathways for electron transfer. To accomplish this feat of mimicry,” says Gust, “we peered over nature’s shoulder, tried something, peered over nature’s shoulder again. Lately, we’ve been going to Neal a lot.”

  Neal Woodbury is a chemist turned photosynthesis sleuth who uses genetic scissors and glue, laser scopes, and millions of bacteria to do his detective work. “Have you seen them?” asks Woodbury, leading me across the hall to the bacteria growth lab. The lab looks like any college biology lab, with long benches and overhead shelves crammed with Bunsen burners and glassware. He squats, reaches below one of the lab benches, and opens the double doors, revealing a series of warm, brightly lit chambers filled with large jars.

  They remind me of the jars you find in country saloons, bobbing with pickled eggs. Some of the jars contain a sludgy brown substance, while others are a mossy green. He moves these aside to find a jar of purple bacterium, Rhodopseudomonas viridis, the color of an Easter egg dye, but thicker. As he holds it up to the light, I see no movement, no sculling backstrokes or twirling whipcords. These bacteria, I remember, are far below my capacity to see, and the jar that Woodbury is holding must contain billions of individuals. As we speak, reproduction and attrition swell and shrink the population.

  For a long time, Woodbury tells me, they had to work from inference, guessing how the cofactors were positioned, because there was no molecular picture of the reaction center. “One of the most dramatic advancements in photosynthesis in this century was to finally get our pictures back from developing and see
a bacterial reaction center molecule by molecule. The reason it took so long is because this assembly we are dealing with is so tiny—taking its picture with something as big as a light ray would be like bouncing a tennis ball against a poppyseed.”

  Instead, scientists had to use small X rays to take the pictures. The technique is called X-ray crystallography, because the molecule to be “shot” is first crystallized—its molecules are lined up so they are all facing the same way, in dress-parade perfection. The X-ray beam passes through the molecule, and the pattern of the diffracted X rays is recorded as an array of spots on a photographic plate. This pattern tells scientists how the atoms are arranged in the molecule—what’s next to what. The toughest part of the process is getting the molecule to crystallize—a protein crystallographer can easily spend eight to fifteen years trying to get a good crystal and picture of one type of molecule.

  The key to getting a good crystal is to completely dissolve the molecules in water first. With proteins that live in membranes, this is no mean trick. Having an affinity for fat (membranes are double layers of fat) but not water, membrane proteins simply clump up in the bottom of a beaker instead of dissolving. It wasn’t until scientists learned to hook water-loving helper molecules to them that the reaction centers were able to blossom in water and finally have their picture taken.

  The scientists who achieved this feat (German chemists Hartmut Michel, Johann Deisenhofer, and Robert Huber) won the Nobel Prize in Chemistry for it in 1988. “Until then,” says Woodbury, “we had been guessing about what elements were in the reaction center, and how they might be oriented in relation to one another. The pictures showed us exactly how nature’s geometry works to enhance the transfer of electrons. Now we have some definite plans to inspire us.”