The Berkeley Science Review: Articles

Photosynthesis
Illuminating Alternatives for Solar Energy Research (view PDF)
by Tracy Powell

You've seen them: matte black, arrayed in regiments, and mushrooming up on what seems like every available outdoor Bay Area surface. From rooftops to traffic signals, solar panels have colonized the landscape—visible symptoms of inexorably rising energy prices and atmospheric CO2.

As this profusion of panels attests, solar energy is booming. Over the past 15 years, demand for solar energy has grown by 30% per year; in 2008 alone, nearly six gigawatts of solar energy-generating capacity were installed worldwide, more than doubling the previous year's installations. Unsurprisingly, as the market for solar energy has expanded, scientists and engineers have intensified their efforts to develop better, more efficient photovoltaic (PV) materials that can convert solar radiation to usable electricity.

To date, the ubiquitous, silicon-based arrays have been the industry standard in solar technology. However, many of these commercial PV materials are bulky, inflexible, and—their cardinal sin—expensive to produce. Better, less costly technologies are needed for solar power to compete with traditional, pollution-generating energy sources.

In pursuit of this goal, some researchers are seeking inspiration from the cheapest, greenest solar-power systems around: plants.

Lean, mean, green machines
Plants have long been central to alternative energy schemes, the push to fill the nation's gas tanks with plant-derived ethanol being a recent example. However, plants' energy significance goes beyond pumping out carbon compounds to be refined into liquid biofuel. Honed by millions of years of evolution, photosynthesis (the process by which plants use solar energy to transform water and carbon dioxide into oxygen and sugars) is a model system for the efficient capture and use of renewable energy. In particular, the efficiency, durability, and flexibility of photosynthetic light-harvesting systems have attracted increasing attention from solar energy researchers.

A leaf may not look a whole lot like a solar panel, but the functional parallels between photovoltaic devices and the early, light-harvesting steps of photosynthesis are profound. Both processes begin with sunlight spilling into the atmosphere. That light, made up of a mixture of different wavelengths, shines onto a reactive surface—a leaf on a houseplant, say, or one of the PV panels encrusting the MLK Student Union.

Upon striking the reactive surface, a few units of solar energy (called photons), carried by light of just the right wavelength, are absorbed. This absorbed energy jolts loose an electron from the reactive surface, and the electron is then harnessed to do work. In a solar cell, it is diverted into a current of similarly liberated electrons, funneled through wires, and eventually used to power all manner of indispensable gadgets that blink and go beep. In photosynthesis, the loose electron instead interacts with a series of biological molecules, eventually driving the chemical synthesis of sugar. Plants and solar energy scientists therefore face a similar task: efficiently transforming light energy into a flow of electrons that can be harnessed to power downstream processes.

At first glance, Mother Nature is no match for the engineers. Commercial silicon PV panels typically convert around 15% of available photons into usable electricity (a statistic called "photon conversion efficiency"); next-generation silicon technologies can exceed 40%. How do plants measure up, those photosynthetic paragons and evolutionary pinnacles of light-harvesting prowess? It is difficult to pin down a parallel estimate, but under full sunlight, a plant only converts around 6% of available photons into electrons. However, on closer analysis, plants' lackluster overall efficiency conceals some very real advantages.

Converting photons into electrons is a multi-step process, the first stage of which is to absorb as many photons as possible from sunlight. Plants are generally confined to absorbing light from the red and blue portions of the spectrum, while photovoltaic materials absorb energy from a wider range of visible wavelengths. (This is why plants look green, while solar cells appear black.) PV materials can therefore reap a bumper crop of photons from each unit of available sunlight, while plants trap a much smaller fraction of available energy. This difference accounts for much of plants' photon conversion inefficiency.

Once photons have been trapped, the absorbed energy must travel to sites where electrons are actually generated and exported. In these later steps of energy conversion, plants can actually outperform solar cells, transporting absorbed energy with near-perfect efficiency. Scientists are therefore probing photosynthetic mechanisms of energy transport, with the goal of using their discoveries to improve the overall efficiency of photovoltaic materials.

In addition to their energy transport efficiency, plants also excel at doing their job on the cheap. They are made out of water, carbon, and a few minerals—all inexpensive, plentiful materials—and they essentially assemble themselves. In contrast, commercial solar panels are constructed of exquisitely pure silicon crystals, whose manufacture is both energy-intensive and expensive. Polysilicon, the bulk material from which PVs are produced, currently costs around $150 per kilogram. At that price, manufacturers are happy to incorporate silicon slivers into consumer electronics; tiling the nation's roofs with the stuff, however, is less feasible. To make solar power competitive, it is widely believed that the retail price of photovoltaic units must drop by 70%.

Many next-generation PV technologies are therefore aimed at reducing manufacturing costs. These advances range from developing cheaper ways to manipulate silicon to replacing it with other inorganic compounds, such as copper or even iron pyrite (fool's gold). Other strategies include using organic dyes, exploring the PV properties of novel nanomaterials, or replacing inorganic solar materials with organic compounds. (Here, organic refers not to your local farmer's market, but to materials made mostly of carbon and hydrogen atoms.)

Though these new PV materials may succeed in dropping manufacturing costs, they have so far been less efficient at converting photons into electrons than traditional, silicon-based devices—organic solar cell researchers, for example, recently trumpeted an all-time conversion efficiency high of just over 6%. Such reduced efficiency might be an acceptable tradeoff for a significantly cheaper technology, so long as the overall cost of generating electricity was lower. Unfortunately, organic and other next-generation PV materials suffer from other problems that have prevented them from realizing their cost-saving potential.

Foremost among their faults, novel PV materials are not durable. Customers would likely object to the hassle of replacing their PV panels (even cheap ones!) on a daily or monthly basis, and continual replacement fees offset any savings gained from using inexpensive materials. Researchers must therefore find ways to extend the lifetime of these novel PV materials. Additionally, even the most promising solar technologies will require innovations in large-scale manufacturing techniques to minimize production and assembly costs.

It is here, in the design and assembly of cutting-edge solar cells, that understanding the biology of photosynthesis becomes relevant. How do biological systems use free, nonpolluting ingredients to produce effective photochemical devices? How do they assemble complex light-harvesting systems under everyday conditions, without elaborate manufacturing techniques? How do they maintain and repair these systems for indefinite periods of time? Researchers are seeking to answer these questions, and hope to one day apply lessons learned from Nature to the rational design of solar energy tools.

Some (self-)assembly required
Cost of manufacture is a major hurdle to commercializing any photovoltaic technology. It's generally safe to assume that if a manufacturing process demands 99.999999999% pure reagents, ultra-high vacuum chambers, and temperatures of 1500û C, it's probably not cost-effective (these, incidentally, are some of the traditional requirements for making silicon wafers). On the other hand, if a PV material can put itself together in a simple, water-based buffer, even die-hard penny-pinchers are likely to give it a big thumbs-up. Such is the logic behind Rebekah Miller's research, which investigates how to exploit the self-assembling properties of biological molecules to build inexpensive light-harvesting structures.

As a doctoral student in Professor Matthew Francis's lab in the Department of Chemistry (she recently graduated and is now at MIT), Miller began her research with tobacco mosaic virus coat protein (TMVP), a simple biological unit that can aggregate into organized structures. Using basic, benchtop reactions, she chemically attached light-absorbing dye molecules to each protein. Once placed in the proper solutions, these modified TMVP molecules assembled themselves into either disks or long, rodlike filaments studded with dye molecules. Because the protein scaffolds fix the dye molecules in close proximity to one another, light energy absorbed by one molecule can easily transfer to a neighbor, allowing the structures to function as light-harvesting, energy-transmitting antennae. Miller's biological self-assembly process had generated functional photovoltaic components.

Miller also showed that combining the dyes in different ratios or changing the combination of dyes used could improve energy transfer efficiency. These results were especially encouraging because they suggested that in addition to successfully harvesting and transmitting light energy, the protein assemblies might offer another benefit associated with biological systems: tunability.

Collectively, plants, algae, and photosynthetic bacteria have evolved a broad repertoire of light-absorbing pigments, including multiple forms of chlorophyll and a large family of molecules called carotenoids. Each pigment absorbs a unique combination of wavelengths, and by combining multiple pigments, an organism can "tune" its ability to absorb light from a preferred range of the spectrum.

Seaweed is a classic example. Millennia of evolution have endowed shallow-water species with green pigments that absorb the red and blue wavelengths abundant in light-rich, surface waters. The red and purple pigments of deep-water species, however, have evolved to absorb the meager, blue-green wavelengths that penetrate the depths. Each species' pigment content has been optimized to absorb wavelengths of light available in their environment. Similarly, to cope with changing light quality on a shorter timescale, many plants can adjust the ratio of different forms of chlorophyll present in their leaves, maximizing efficient light use.

This flexible approach to light absorption appeals to engineers. Just as photosynthetic organisms rely upon a variety of biological pigments, researchers have developed many synthetic pigments, each of which absorbs a unique spectrum of light. By mixing and matching the pigments shackled to her TMVP structures, Miller's assemblies could one day be optimized to expand the range of wavelengths from which they can harvest light, greatly enhancing their flexibility and efficiency.

Currently, researchers in the Francis lab are working to combine TMVP light harvesting antennae with small molecules that can conduct electricity, with the goal of designing functional electronics that operate like biological systems. On a more basic level, studying the behavior of these assemblies could help improve our understanding of how light energy is transmitted on the small spatial scales relevant to PV design.

However, despite the potential advantages in cost, tunability, and manufacturing simplicity, directly incorporating biological components into photovoltaics would also bring special challenges. Primarily, biological molecules tend to degrade quickly, particularly under high-intensity light. According to Miller, preliminary evidence suggests that the three-dimensional structure of the TMVP scaffold may help to stabilize it, protecting the assembly against light-induced decay. Nonetheless, the overall vulnerability of organic PV components has led scientists to search for better mechanisms to protect them—a search that has led to closer examination of how biological systems maintain themselves under challenging environmental conditions.

Do-it-yourself fixer-upper
It doesn't matter whether you're a plant or a PV engineer—if you lavish time, effort, and precious resources on constructing a light-harvesting system, you want it to last. Unfortunately, components in both natural and manufactured photosystems degrade over time. Organic solar cells, for instance, rarely last more than a single day. The chemical reactions that lead to this decay are not always well understood, but oxidation (the same oxygen-dependent process that rusts your car and browns your apples) is a likely culprit. Simply by isolating it from oxygen, an organic PV's lifespan can be extended from days to weeks.

Similarly, in plants, key photosynthetic proteins can be damaged or destroyed by oxidation within minutes of activity. At noon on a sunny day, for instance, plants are bombarded with high-energy photons. This light energy is temporarily absorbed by chlorophyll molecules, rendering them chemically volatile until they have passed the energy off to other acceptor molecules. Under low-intensity light, this handoff is rapid: energy is immediately siphoned away and expended in controlled, downstream chemical reactions. But when light is intense, the plant's photosynthetic machinery can be overwhelmed. A backlog of absorbed energy builds, and excited chlorophylls have nowhere to expel their excess energy. These dangerously reactive chlorophylls can then spawn destructive oxidative reactions that cripple proteins, damage membrane components, and generally wreak havoc in the cell.

Fortunately, plants have evolved an array of clever mechanisms to shield themselves from the oxidative dangers of photosynthesis. To learn more about these protective strategies and whether they might be adapted for solar cell design, chemists and biologists are collaborating to understand fundamental protective mechanisms. Of particular interest is a pigment called zeaxanthin (pronounced zee-uh-ZANTH-un).

Zeaxanthin has long been known to stifle (or "quench") chlorophyll's hazardous chemical reactions under high-intensity light. However, "the exact mechanism for this kind of quenching was not well studied," explains Tae Ahn, a postdoctoral fellow in Professor Graham Fleming's chemistry laboratory. Frustrated by the fragility of organic photovoltaics in his graduate research, Ahn became interested in zeaxanthin as a potential model for protective energy quenching in next-generation PV materials.
To better understand how zeaxanthin protects the plant, Ahn first wanted to identify exactly where its quenching activity occurs. This was no trivial task. Textbook diagrams may reduce photosynthesis to a parade of comfortably spaced cartoon blobs, but in reality this process transpires in dense, dynamic rafts of proteins, swaddled in membrane and cloistered in the deepest recesses of the chloroplast. Zeaxanthin could be interacting with any of hundreds of these molecules. Furthermore, its quenching reaction lasts mere trillionths of a second. Pinpointing the exact site of this ephemeral process required some serious sleuthing.

To narrow the hunt, Ahn collaborated with Roberto Bassi, a biochemist at the University of Verona, Italy, who had purified several photosynthetic proteins suspected of interacting with zeaxanthin. (This in vitro approach removed much of the biological bric-a-brac that obscures quenching behavior in the plant cell itself.) Ahn then used a technique called ultrafast pump-probe spectroscopy to identify which of the purified protein candidates facilitate zeaxanthin's protective quenching. In keeping with its impressive name, this method offers the ultimate in laser-light machismo: fast, powerful, exquisitely controlled lasers bombard a sample with light. An initial "pump" pulse of laser light triggers a chemical reaction in the sample—in this case, exciting a chlorophyll molecule bound to a sample protein. Subsequent laser pulses (the "probes") are delivered a few trillionths of a second later, and allow researchers to collect information about how the sample has changed as a result of the initial pump stimulus. Because data can be collected over minute increments of time and space, researchers can actually track physical and chemical reactions as they occur. Ahn's spectroscopy experiments therefore allowed him to watch photosynthetic proteins absorb light energy, then measure whether or not zeaxanthin could stabilize the excited chlorophylls in a quenching reaction.

Using this method, Ahn first narrowed down which of several protein clusters participated in quenching. He showed that the major light-harvesting antenna (one important complex of photosynthetic proteins) did not undergo quenching after laser excitation, indicating the proteins that compose this complex did not participate in zeaxanthin's protective efforts. However, after an initial zap with the laser, three proteins from a second cluster, called the minor light-harvesting antenna, did facilitate quenching. From a daunting lineup of potential candidates, Ahn had identified three proteins responsible for quenching: CP26, CP29, and CP43.

Working from this preliminary identification, Ahn collaborated with Tom Avenson, then a postdoc in Krishna Niyogi's lab in the Department of Plant and Microbial Biology, to further pinpoint the mechanism of quenching. Focusing on CP29 as a case study, Ahn determined that in order for quenching to occur, the protein must be able to bind two chlorophyll molecules very near to zeaxanthin. This suggests that, in periods of high-intensity light, physical proximity allows zeaxanthin to donate an electron to this nearby pair of over-excited chlorophylls—a chemical mechanism that could stabilize its chemically volatile neighbors.

When asked about immediate applications of this knowledge to PV design, Ahn
acknowledges that practical implementation is a distant prospect. However, he suggests that solar energy researchers might one day mimic plants' protective mechanisms by seeding PV materials with molecules that prevent degradative chemical reactions (like zeaxanthin).

In a more general sense, a better understanding of how photosynthetic energy conversion can be controlled at such small scales could also improve PV design. Fleming, for instance, has likened zeaxanthin's quenching activity to a protective dimmer switch. By clarifying how this molecule regulates the flow of energy through the photosynthetic protein complex, his group hopes to improve scientists' control over the behavior of energy generated by PV devices. Indeed, to better understand energy fluxes in plants, researchers in the Fleming lab have looked beyond purely protective mechanisms and applied their advanced spectroscopic techniques to other important steps of photosynthesis.

A quantum of sol
One question to which Fleming and his collaborators have applied their expertise is understanding what happens to solar energy once it has been absorbed by the plant. Based purely on photon absorption efficiency, plants do a relatively shabby job of harvesting the photons available in sunlight. However, once a photon is absorbed, its energy is transferred to electrons with remarkable efficiency—approximately 97%. By comparison, PV materials typically only achieve 20-90% energy transport efficiency once light energy is absorbed. Understanding how biological systems manage such energy thrift could therefore inspire efficiency breakthroughs in artificial photosynthetic systems.

Plants have evolved a specific architecture to support efficient energy transfer, packing light-absorbing chlorophyll pigments into protein clusters called antennae. Photons of light are absorbed in the antennae, and the resulting energy hopscotches from one chlorophyll molecule to the next until it reaches another protein complex called the reaction center. Here, the energy finally escapes in the form of an electron, and is used to power downstream chemical processes like making sugar.

To make solar energy conversion as efficient as possible, absorbed energy must seek the shortest, speediest escape route from the antenna to the reaction center. Until recently, researchers usually depicted this escape as you would any normal biochemical phenomenon: as a linear, stepwise process. Like a mouse in an unfamiliar maze, they believed the energy of an absorbed photon would make arbitrary "decisions" about which nearby chlorophyll to jump to, arriving at the reaction center only after a series of twists, turns, and backtracking.

However, this assumption never entirely made sense. Photosynthetic energy capture is simply too efficient for energy to aimlessly meander between chlorophylls. In a sequential process like that, energy would leak away at every step. How could such inefficient hopping permit near-perfect energy efficiency?

In a 2007 paper in Nature, Greg Engel, then a Miller Postdoctoral Fellow working with the Fleming laboratory, presented evidence favoring an alternative explanation. What if, instead of the traditional stepwise model, quantum physics could explain photosynthetic energy efficiency?

In the weird, subatomic world of quantum physics, energy doesn't behave as a single, concrete unit—energy doesn't bumble sequentially from one place to the next. Rather, it simultaneously inhabits a variety of locations, its distribution smeared across many probable sites. Only when a particular event, such as a chemical reaction, forces it to attend a defined location does it manifest at that site.

According to this model, excitation energy absorbed by a light-harvesting antenna would spread out to simultaneously occupy all of the intervening chlorophyll molecules en route to the nearest reaction center. Only when chemical events at the reaction center require the energy to be located right there, just then, does this fuzzy distribution snap into a single, linear path—the shortest distance between antenna and reaction center. It is as if the most efficient path is calculated retroactively. Engel sought to discern whether this sort of quantum process permitted the efficiency of photosynthetic energy transfer.

To test whether the quantum model was correct, Engel and his collaborators purified a glob of proteins normally sandwiched between the antenna and the reaction center of photosynthetic Chlorobium tepidum bacteria. The group had previously shown that these proteins act as a biological wire, conducting energy as it travels to the reaction center. This time around, they wanted to stimulate the proteins with light and then observe the exact pattern of energy in transit, hoping to determine whether it exhibited quantum behavior.

Using a variation of the same laser spectroscopic technique used by Ahn, Engel and his colleagues tracked how energy spread throughout the sample. They observed "quantum beats," a distinctive pattern of energy spikes that propagated through the excited proteins. Just as two pebbles plunked into a pond will produce intersecting sets of ripples, these quantum beats are formed by the interactions between wavelike energy pulses of absorbed photons. Crucially, this pattern could not have been generated by stepwise energy transfer; it is distinctly characteristic of quantum events, in which energy distributions assume a wavelike form.

Since these findings were published in 2007, coauthor and Fleming lab graduate student Tessa Calhoun has continued the project. Using the same spectroscopic approach, she has observed quantum energy transfer in the light-harvesting complexes of higher plants, which are significantly more complicated than the simple bacterial clusters used in the initial study. As a result of this research, quantum energy transfer is emerging as an important paradigm in PV research.

Such fundamental understanding of how biological systems promote efficient energy transfer lays the groundwork for vast improvements to solar technology. Today, for example, solar cells rely on simple diffusion of charged particles to transport absorbed solar energy to a conductive surface. Future PVs might instead mimic plants' separation of light-harvesting and electron-donating functions—improving performance by efficiently shuttling light energy from antenna structures to a synthetic reaction center.

This sort of advance could redefine the very nature of photovoltaic materials. "Traditional photovoltaic materials, such as silicon, tend to be very ordered," explains Engel, now an assistant professor at the University of Chicago. "In contrast, photosynthetic systems are very disordered, with much more elaborate architecture at the molecular level. Using what we're learning about how such biological complexity supports energy transfer, we're now attempting a more sophisticated approach to designing photovoltaics."

Green revolution
From self-assembly and protective quenching, to the quantum mechanics of energy transport, photosynthesis is poised to inspire PV innovation in many different ways.

Some researchers embrace photosynthetic processes as an inspiration, but suggest that the fragility and complexity of biological photosystems preclude their direct use in large-scale solar power endeavors. Both Ahn and Engel, for example, embrace photosynthetic processes as inspiration for
next-generation photovoltaic design principles.

In contrast, other researchers have sought to exploit biological materials despite their shortcomings. The Francis lab, for instance, continues to build upon Miller's work with TMVP light-harvesting assemblies. In another example, the mechanical engineering department's Liwei Lin has used isolated bacterial photosynthetic membranes to directly power microscopic electronic devices (see BSR Spring 2007).

In the crowded field of next-generation photovoltaics, it is yet unclear which technologies will prevail. Nonetheless, one thing is certain: from plant-inspired designs to solar devices that actually derive power from photosynthetic proteins, the future of solar energy has never looked greener.

Tracy Powell is a graduate student in plant and microbial biology.

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