by Diane Boudreau
Stretch your imagination back about 2.5 billion years. The Earth was a younger, more desolate planet in those days. Its barren surface was bombarded with intense radiation from the sun. The atmosphere was a toxic cocktail of methane, carbon dioxide, hydrogen sulfide, and ammonia.
In this hostile environment, life somehow took hold. Protected from the sun in acidic oceans, single-celled bacteria began to thrive. Unlike all living things to follow, these bacteria lived in an environment with no free oxygen. They enjoyed a steady diet of hydrogen sulfide, the substance that gives sewage its memorable odor.
Life might have continued on this way if not for the clever cyanobacterium. Perhaps a shortage of hydrogen sulfide forced cyanobacteria to find nourishment somewhere else. Whatever the reason, they developed a new process for harnessing the sun's energy by splitting water molecules instead of hydrogen sulfide. In doing so, they caused the world's first environmental disaster. They also made life as we know it possible.
Their revolutionary process was aerobic photosynthesis. This is the type of photosynthesis most of us are familiar with. It involves using the sun's light to break water molecules into hydrogen and oxygen, capturing energy in the process.
The oxygen we breathe is a byproduct of photosynthesis. Ironically, the oxygen we need to survive was poison to the older bacteria that once dominated the Earth.
Now let your imagination snap back to the present like a rubber band. As you whiz through the eons, life on Earth changes drastically. Plants begin populating the land. The oceans birth the first animals. These animals develop lungs and creep out of the seas.
Giant reptiles rule the Earth for millions of years before suddenly going extinct. Primates climb down from the trees and walk on two legs. They learn to talk and build houses, write books and make sculptures, and even study how they got here in the first place.
Through it all, photosynthesis has remained almost exactly the same.
Scientists at Arizona State University are looking to photosynthesis to help us with our most recent environmental crisis.
"We're all addicted to oil," says Thomas Moore, director of ASU's Center for the Study of Early Events in Photosynthesis and professor of biochemistry. "We are starting to see the effects of energy insecurity. Developing sustainable energy sources may be the most serious problem we've ever faced."
Oxygen once made our planet hostile to existing life forms. Now carbon dioxide threatens to do the same. Mass burning of fossil fuels has drastically raised carbon dioxide (CO2) levels in the atmosphere, raising global temperatures along with it.
No one is certain what the exact effects of this will be. Even slight changes in temperature can change ocean levels and acidity, shift animal habitats, and affect crop growth. All of these changes would have an impact on human health, security, and economics.
Our oil addiction also leaves us dependent on nations that aren't always friendly to the United States. Even if they were, the supply of fossil fuels is limited. You can't simply plant new oil beds and expect to reap the rewards in a few years or even centuries. Coal will last longer, but it pollutes even more than oil–think about the soot-filled skies of a Dickens novel.
"If you look for a sustainable source of energy that doesn't produce CO2, the only thing that's practical right now is solar. The only thing there is enough of to satisfy all our power needs is sunlight," says Devens Gust, a professor of organic chemistry who studies renewable energy.
We already use solar power to some extent. A small fraction of Arizona's electric power is generated through solar panels, for example. But current solar technology has its limitations. Solar panels are very expensive. They also only produce electricity when the sun is shining–homes that use solar panels still need an alternative energy source for nighttime power needs. Finally, solar panels can produce electricity, but they can't power a car or an airplane.
"Electricity only accounts for 20 to 30 percent of U.S. energy use," explains Moore. "Most of our energy use is for transportation, which is also the main producer of carbon dioxide."
Most transportation relies on fuel, not electricity. To run cars and trucks and planes on solar power you have to capture and store the energy. Scientists haven't found a very efficient way to do that yet. But plants have.
"Photosynthesis is obviously here and it obviously works," says Gust. "It powers all organisms on Earth, either directly or indirectly. All our fossil fuels come from photosynthesis."
ASU is home to one of the largest groups of photosynthesis researchers in the world. With so much expertise on the subject, ASU is a logical place for applying basic knowledge of photosynthesis to the energy problem.
The researchers are approaching the issue from different angles. However, they are all working towards the same goal–harnessing the power of the sun to produce clean, cheap, renewable energy. Because plants already know how to do this remarkably well, it makes sense to study their method in the hopes of mimicking–or maybe even improving–it.
The power of green
A plant's leaf is a natural solar cell. Leaves capture light energy using pigment molecules called chlorophyll. Chlorophyll is what makes plants green. The chlorophyll acts as an antenna, catching the sun's rays and funneling its energy into a reaction center that splits water molecules into oxygen, hydrogen ions, and electrons. This reaction center is called photosystem II. The energy then gets passed to another reaction center–photosystem I–where it is used to combine CO2 and hydrogen to form carbohydrates, a type of fuel.
It is a perfect system. Plants use unlimited light energy to split water. Then they convert that energy into a fuel that can be stored and used when needed. The only "waste" product is oxygen.
Petra Fromme is trying to figure out exactly how this system is designed. The ASU biochemist studies the structures of photosystems I and II in the hopes of understanding how they work.
Fromme led the research team that first crystallized and imaged the two photosystems. Crystallizing the molecules allows scientists to study their function. By shining X-rays through the crystals and studying the diffraction patterns they create, Fromme and her colleagues can determine their structures. The process also leaves the photosystems active. By shining light on the systems, the researchers can actually watch reactions happen in the single crystals.
Fromme's first images of photosystems I and II were published in Nature in 2001. The results provided some surprises.
"Before we crystallized photosystem I, everyone expected the chlorophylls to be in a ring, but they're not. It's more like nerves in your brain. They are all connected, but not in a ring," she says.
It turns out the layout of the chlorophylls–which looks random at first glance–makes the system more robust.
"If you have a ring and one piece fails, then the link is broken," she explains. Instead, the system offers multiple pathways for the energy, so that if one piece fails, energy can be transferred a different way. In addition, the chlorophylls are oriented in different directions, so they can receive as much light as possible.
"The chance that energy will be transferred from any chlorophyll is 99.9 percent. It's extremely efficient and extremely robust," says Fromme.
And it isn't random. The arrangement of chlorophylls may appear chaotic, but it is exactly the same in all plants.
"Photosystem I in cyanobacteria has almost the exact same structure as photosystem I in higher plants. It looks random, but it isn't. It has been highly conserved over 1.5 billion years," Fromme says.
Currently, Fromme has turned her attention to a particularly elusive–but essential–piece of the photosynthesis puzzle. A plant's ability to break apart water molecules depends on a cluster of four manganese atoms known as the "oxygen-evolving complex."
"To crystallize this structure is a nightmare," Fromme says. "When you isolate photosystem II, the first thing damaged is the manganese cluster. Before we solved the first structure, it had never been crystallized in an active state."
The work is not finished, however. Researchers still cannot visualize the individual manganese atoms. As a result, no one knows the exact structure of this complex, so they can't just build it for themselves.
Even if they could, they might not be able to make it stable. The manganese cluster is attached to a protein that is highly unstable because of its proximity to oxygen, which can become reactive and damage the molecules around it.
Oxygen is both a blessing and a curse. It gives us life, but also takes it away. Oxygen's damage to human cells ranges from cataracts to cancer. In plants, the protein in photosystem II has a life span of only a half-hour because of oxygen damage. The plant must constantly replace that protein in order to function.
"This is a 2.5 billion-year-old enzyme, but nature hasn't solved the problem with this damage," says Fromme.
Strangely, the protein is more stable in crystallized form. After a half hour, the crystallized protein shows only 10 percent damage instead of 90 percent.
Fromme continues to try to image the oxygen-evolving complex in its active state. She has a grant from the National Institutes of Health to try to produce a high-resolution image of the complex. She wonders if scientists might be able to improve the stability of the complex in a synthetic form of photosynthesis.
Light activated assembly and repair
Neal Woodbury is giving that challenge a try. He is working to develop a molecule that functions like the oxygen-evolving complex.
"A number of us are interested in this problem—converting either sunlight or another form of renewable energy into fuel," says Woodbury, a professor of biochemistry who works with the Photosynthesis Center. "The basic issue there is catalysis."
A catalyst is a substance speeds up a chemical reaction. The catalysts generally used in biology are proteins called enzymes. Photosystems I and II provide the power for the enzymes that make sugars and break down water molecules.
"Students in any high school class can stick two electrodes in water and make hydrogen," says Woodbury. "But it's an inefficient process, and a lot of energy is wasted as heat. The oxygen-evolving complex does this reaction much more efficiently than an electrode. Can we adapt the chemistry from that for an artificial catalyst?"
Using basic knowledge of photosynthesis from scientists like Fromme, Woodbury is trying to custom-build enzymes that will do the work of photosynthesis. The enzymes will either take their power from renewable sources of electricity–like solar panels–or directly from light if used with an artificial reaction center.
Photosynthetic enzymes are also self-assembling and self-replicating. In most biological systems, proteins do the construction work. In the photosystems, however, assembly is light-activated. The ability to self-repair is critical for proteins like the one in photosystem II that needs to be replaced every half hour. The scientists at ASU will have to figure out how to make their enzyme more stable, or else create one that self-replicates.
"This is why we want to see the structure of the manganese complex in different oxidation states," says Fromme. "We want to understand how native systems work and then maybe make a synthetic system. You cannot replace proteins constantly in an artificial system."
"The problem with natural enzymes is that they're very complicated molecules, with tens of thousands of atoms," adds Woodbury. "We are making artificial enzymes. They are smaller, simpler, but contain the essential elements of nature's enzymes. The process involves building and then testing 100,000 different types of molecules at the same time."
Nature's "research methodology" involves making lots of stuff randomly and allowing the successful experiments to survive, while the unsuccessful die out. This process, of course, takes a very long time.
"We don't have 100 million years like nature did," explains Woodbury. "So we are applying our computers and knowledge of chemistry and hoping to condense it to a few years."
The process is called combinatorial chemistry. The researchers don't know the exact structure of the oxygen-evolving complex. So they create computer models based on what they do know about how metal binds with protein. Then they will produce massive numbers of peptides–pieces of proteins–and test them for effectiveness.
"You start with a guess, then you screen massive numbers of peptides and you test each one," says Jim Allen, an ASU biochemist involved in the project. "In combinatorial chemistry, you screen lots of related compounds. The hope is that we'll get close enough to see systematic improvement in the quality of what we're measuring."
The end product might not be exactly the same as the natural oxygen-evolving complex, but that's okay.
"Whether our assay is the same as plants is less critical than whether it works," Allen explains. "We know what to test for, and that's what makes it feasible to try."
Building molecules in Woodbury's lab is a lot like building computer chips.
"We have the same problem the computer industry had years back," he says. "It got to the point where you couldn't put something complex together with a soldering iron. This was solved by patterning chemistry. You shine light on plastic to polymerize it in certain places. Then you can put metal or semiconductor on the spaces between. It's built layer by layer. You don't place a transistor there–you build it in place."
Woodbury's chips don't hold transistors; they hold molecules–peptides, to be specific. But he isn't restricted to using peptides that occur in nature. In fact, he's creating entirely new ones.
"It's like a big Lego set," he says. "The computer controls which piece gets stuck on the Lego. The term 'click chemistry' describes pieces that come together quickly. I call this 'photoclick chemistry,' using light to put the pieces together."
Allen and ASU chemist Joanne Williams design peptides for the project. Trevor Thornton, a professor of electrical engineering, navigates the technical intricacies of producing chips. So far the researchers have tackled the technical issues of putting the pieces together. Soon they will begin testing potential enzymes for effectiveness.
DNA origami
Peptides aren't the only things you can custom-manufacture. While Woodbury tinkers with peptide "Legos," Stuart Lindsay makes origami with DNA. The technique, which is actually called "DNA origami," lets the ASU biochemist bend strands of genetic material into all kinds of different shapes. His goal is to create a DNA scaffolding that will hold a complex antenna system similar to the ones used by plants.
In plants, the chlorophyll actually focuses, transfers, and absorbs light energy. Lindsay's system will divide the labor. Silver particles will capture and focus the light on separate dye molecules that then absorb the light.
"There are molecular solar cells in existence but they aren't very efficient," Lindsay explains. "You need a big long row of dye molecules to absorb all the light. We're proposing to make nanoscale antennas to collect and focus light more efficiently and radiate dyes with very intense light. You can make a single layer of dye absorb all the light this way," he says.
"The reaction center itself can't absorb efficiently in normal sunlight," adds Gust, who also works on the project. "The antenna has lots of light absorbing molecules. It catches light and feeds it to the reaction center. The antenna keeps pumping light and photons at a rate that lets the reaction center work efficiently."
The first step in building an antenna system is to design the structure of the DNA scaffolding on a computer.
"You bend the DNA by using short bits of DNA with 'sticky' ends to fasten two sections together," Lindsay explains. "You pick out where to crosslink two strands together and then find the DNA that will connect there. Out from your computer comes a little ordering list, saying, 'You need these bits of DNA.'"
After that, he puts the strand of DNA in solution with the sticky bits, heats it all up, cools it down again and–voila!–custom DNA shapes.
"It's an unbelievable process," says Lindsay. "What's marvelous is you can make self-assembling structures of DNA that have single strands poking out, like a tether line."
In fact, Lindsay and Hao Yan, a professor of inorganic and materials chemistry, created the first addressable nanoarray–an array with strands sticking out at specific locations. As an example, they created a nanoarray that spells out "ASU" using protruding DNA loops.
Making words out of DNA is fun, but the process is functional as well. The protruding bits can serve as attachment points for specific substances. In the case of an antenna system, Lindsay will attach the silver particles that will capture and focus light.
Plants use the sun's power to make sugars. If scientists can mimic photosynthesis, they will not be limited to making carbohydrates. They could instead take the hydrogen from water and use it as fuel.
The potential for a "hydrogen economy" is big news these days because hydrogen is plentiful and burns very clean. The only byproduct is water. However, a hydrogen economy would require major infrastructure changes. Hydrogen is difficult to transport because it is highly flammable. Also, hydrogen fuel cell technology is still immature. Current fuel cells aren't very efficient, but researchers around the world are working to improve them.
Another option is to replicate photosystem I and use the energy released from splitting water to make carbon-based fuels. Sugars are great for powering our bodies, but other carbon compounds, such as methanol, ethanol, butanol, methane, or lipids might be able to fuel our cars.
Carbon-based fuels release carbon dioxide when they are burned, but they would use up that CO2 by being created photosynthetically. Using these fuels would not add CO2 to the atmosphere.
Certain carbon-based fuels might work better with our current infrastructure than either hydrogen or other carbon-based options. For example, some forms of fuel cannot be pumped through existing oil pipes, but others can.
Moore says that sustainable energy is likely to develop in many forms. There are researchers working to improve solar panels and fuel cells. Still others are developing biomass, which relies on natural rather than artificial photosynthesis (see sidebar). Some researchers are developing better technology for harnessing other renewable resources such as wind or geothermal energy.
"I think the world is coming to realize a sustainable source of energy is a crucial issue facing humans," says Moore. "There won't be one way, there will be a number of ways linked to local resources. For example, in Iceland, geothermal energy is abundant. That's not practical in other places. There are places with a lot of wind, places with a lot of sun. This is a model for energy that's different from what we had in the past, which was large, centralized sources of energy."
Here in Arizona, which boasts more than 300 sunny days per year, studying every facet of solar power only makes sense. But while scientists can develop and improve ways to harness energy, no one can use their technology unless policy supports it. The legislators and voters will ultimately decide if and how to feed our hunger for power in a way that can be sustained for the long term.
Photosynthesis-based energy research at ASU is supported by the U.S. Department of Energy, the National Science Foundation, and the National Institutes of Health. For more information, contact Thomas Moore, Director of the Center for the Study of Early Events in Photosynthesis, 480.965.3308. Send e-mail to: tom.moore@asu.edu
