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From Biomimesis to Bioinspiration: What’s the Benefit for Solar Energy Conversion Applications? Valentine Ivanov Vullev* Department of Bioengineering, Department of Chemistry, Department of Biochemistry, and Center for Bioengineering Research, University of California, Riverside, California 92521, United States ABSTRACT: Ever-growing global energy consumption, along with climate threats involving anthropogenic activities, places a premium on sustainable and environmentally safe energy sources. Solar radiation reaching the Earth’s surface delivers energy at a rate that considerably surpasses the current and projected rates of global energy consumption. Through the millennia of evolution, photosynthesis evolved to harvest solar energy and utilize it for the anabolism of caloric substances that are stored and used as biological fuels. Therefore, the photosynthetic systems are excellent paradigms for solar energy science and engineering. Mimicking photosynthesis provides a means not only to further the solar energy conversion science but also to test and elucidate key aspects of the biological light harvesting. Concurrently, inspiration from the biological and biomimetic advances is a key driving force in the development of solar energy conversion applications. This Perspective presents a view of the role of biomimesis and bioinspiration in meeting the demands for energy and sustainability.
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arvesting Solar Energy. On the verge of anthropogenic climate change, civilization’s successful evolution out of the fossil fuel age will depend on technologies that use carbon-free energy sources to meet the world’s energy demands.1,2 Among the candidate technologies, solar light has the unique potential to sustain the ever-growing energy needs of humanity in the most environmentally benign manner.3 With an average flux at about 160 W m-2, solar radiation reaching the Earth’s surface offers energy at a rate that is orders of magnitude larger than the rates provided by other primordial energy sources such as geothermal gradient, atmospheric electric discharge, and radioactivity.4 The evolution of photosynthesis has made it possible for the life on our planet to flourish from the abundant sunlight as a sustainable energy source. In fact, via millennia of photosynthetic processes, plants and diatoms stored solar energy in a form of organic mass to produce fossil fuels,5 that is, the coal and the oil that have driven industrial development for more than 100 years. While Alexandre-Edmond Becquerel discovered the photovoltaic effect at the beginning of the 19th century,6 solar cells still make a negligible contribution to the world’s energy production in comparison with fossil fuels.7 Conversely, for about three billion years or more, solar energy sustained life on Earth via photosynthesis.8,9 The efficiency of photosynthetic conversion of sunlight to usable energy is only a few percent. This seemingly low energy conversion efficiency is more than sufficient for sustaining organisms through photosynthesis8,9 but, so far, is not adequate to compete with “traditional” energy sources. Nevertheless, the light-harvesting “machinery” that resulted from eons of evolution presents an excellent learning paradigm for capturing and storing solar energy (Figure 1).10,11 Biomimetic versus Bioinspired: What’s the Difference? At first glance, the terms biomimetic and bioinspired appear interchangeable. r 2011 American Chemical Society
Biomimesis and bioinspiration, however, carry different denotations and connotations, and as such, their implications for science and engineering also differ. The term biomimetic (also referred to as bioimitating), which was introduced in the 1970s,12 suggests imitation of biological
Biomimesis and bioinspiration carry different denotations and connotations, and as such, their implications for science and engineering also differ. systems. Through decades of research, biomimetics allowed us to examine our understanding of biological systems at molecular, organelle, cellular, tissue, organ, and organism levels. As “working models” of their biological counterparts, biomimetics provide venues for unambiguous tests of structure-function relations without dealing with the complexity of the living systems. The process of biomimetic design also tests our understanding of how biological systems function. The extent of expected functionality, achieved via simplified imitation of living systems, reflects the depth of comprehension of the factors that govern the investigated biological processes. Received: November 28, 2010 Accepted: February 4, 2011 Published: February 15, 2011 503
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Figure 1. Light energy harvesting through photosynthetic machinery self-assembled on a thylakoid membrane. The presented thylakoid suborganelle is a simplified representation and not to scale (decreased dimensions), in comparison with the surface-modeled proteins from their respective crystal structures obtained from the RCSB protein data bank (PDB). On the basis of the availability of high-resolution structures, the shown proteins are from different organisms. Following the electron-transfer chain, the proteins and their PDB IDs are (1) photosystem II (PS II), cyanobacterial monomeric crystal structure (PDB ID 3KZI); (2) cytochrome b6f (Cyt b6f), cyanobacterial crystal structure (PDB ID 2ZT9); (3) plastocyanin (Pcy), plant crystal structure (PDB ID 1AG6); and (4) photosystem I (PS I), plant crystal structure (PDB ID 3LW5). Splitting water by the oxygen-evolving complex at PS II and oxidation of plastoquinol (PQH2) by Cyt b6f complex releases hydrated protons in the lumen, generating a pH gradient across the thylakoid membrane, which powers the ATP synthase (ATPase) (yeast crystal structure, PDB ID 2XOK) to convert ADP to ATP. The generated reduced electron/proton carrier (NADPH) and ATP in the light reaction pathway are consumed in the dark reaction pathway (Calvin cycle) to convert CO2 into a simple sugar, glyceraldehyde-3-phosphate (G3P), which is a precursor for higher-molecular-weight carbohydrates, fatty acids, and amino acids.
While biomimetics play a crucial role in exploratory research and in basic science, their technological implementations are somewhat limited. The translation from basic to applied science and from exploratory to developmental research is where bioinspiration takes over. Bioinspired systems, which adopt ideas and principles from biology without apparent resemblance to the biological paradigms, provide a liaison between basic science and applied engineering. Bioinspired engineering requires an understanding of how the living systems work. The design and engineering of bioinspired systems, however, allow for adding characteristics that are not available in their biological models. Thus, it is possible to engineer a bioinspired system with performance superior to that of a living or biomimetic system. While biological systems have evolved to sustain organisms, they do not necessarily provide the best answers to technological demands. Going beyond what Nature provides usually entails a number of transitions, (1) from biomimicry, which involves solely superficial imitation of the biological systems, (2) to biomimesis, which attempts to copy and recreate the structurefunction relations observed in living entities, and finally (3) to
bioinspiration, through which structural properties and functionality are pushed to new levels, beyond what Nature offers. This evolution of technological concepts, undoubtedly, creates gray areas that explain some interchangeability of the terms biomimetic and bioinspired. Such gray areas are especially representative for systems in which the application development commenced while the successful imitation and comprehension of certain aspects of the biological paradigms are still incomplete. Incidentally, the term bioinspired entered the scientific literature about two decades after the introduction of the term biomimetic.13 Although the terms biomimetic and bioinspired are only a few decades old, biomimicry, biomimesis, and bioinspiration have been inseparable components of the technological progress through the centuries. For example, through bioimitation and bioinspiration, we learned how to fly and how to ease human labor by the advancement of robotics and, eventually, by the expected inception of artificial intelligence. Therefore, it is only reasonable to turn to biomimesis and bioinspiration in the pursuit of solar energy as a source for technological sustainability. Mimicking Photosynthesis. Through a series of energy-transfer, charge-transfer, and synthetic steps, photosynthesis converts 504
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captured solar radiation into chemical energy. The high-energy adenosine triphosphate (ATP), formed from a photosynthetically driven pH gradient, is the universal fuel source for life. In addition to generating a pH gradient responsible for driving ATP synthesis, the tandem function of photosystem II (PS II) and photosystem I (PS I) powers photocatalytic splitting of water that results in the anabolism of nicotinamide adenine dinucleotide phosphate (NADPþ) to its reduced form, NADPH, with concurrent oxidation of water to yield oxygen in a separate compartment (Figure 1). The Calvin-Benson cycle utilizes the harvested solar energy (ATP via oxidative phosphorylation of ADP driven by the photogenerated pH gradient and NADPH via ferredoxin/NADPþ oxidoreductase in PS I) for the assimilation of carbon dioxide to reduce it into glyceraldehyde-3-phosphate (G3P). G3P is a precursor for a range of higher-molecular-weight carbohydrates that, in addition to being key building blocks for biological supramolecular structures, are important fuel for relatively long-term energy storage in living organisms. Hence, the overall chemical and energy balance of plant photosynthesis represents the use of solar energy for conversion of water and carbon dioxide into an oxidant (oxygen) and fuel (carbohydrates), making the photosynthetic machinery an essential paradigm for developing sustainable energy technologies (Figure 1).
The role of the protein templates, however, extends beyond the sole maintenance of the structural integrity of the arrays of photoactive redox moieties. The electronic coupling provided by polypeptide chains,18-20 the redox properties of the amino acid residues,21 and the local electric field gradients from the intrinsic dipole moments of the peptide bonds and other polar groups22-24 have a key mechanistic impact on charge-transfer processes occurring in polypeptide self-assemblies mimicking the protein environment.25 Furthermore, when driven by cooperative weak interactions (rather than covalent bonding), self-assembly of chromophore arrays, templated by proteins, for example, has a crucial advantage for self-repairing processes that are essential for living systems susceptible to photodamage. For photovoltaic engineering, it is essential to mimic (1) the large effective cross section for the light absorption by the antenna chromophore arrays, (2) the energy transfer to the special pairs of the PRCs, and (3) the long-range photoinduced charge separation mediated by the PRCs (with a quantum yield of unity). By itself, the long-range photoinduced charge separation, however, does not provide means for storing the harvested solar energy. Mimicking the processes of water splitting and carbon dioxide fixation provides this missing link in solar energy conversion. The photocatalytic splitting of water, mediated at inorganic interfaces, has been known for almost half of a century.26 The enzymatically catalyzed reduction and oxidation of water, however, still provide the most elegant ways for avoiding extreme pHs and single-electron (energetically unfeasible) intermediates. Furthermore, the enzymatically aided photosynthetic water splitting is driven by energy corresponding to the visible and the nearinfrared regions of the spectrum. In higher photosynthetic organisms, the formation of NADPH evolved to be the feasible way for storage of reduced hydrogen. For industrial use, however, molecular hydrogen appears to be the preferred product from water reduction because it can be used in the current technological infrastructure based on combustion processes. Therefore, hydrogenases, which are enzymes responsible for reversible formation of H2 in certain microorganisms, provide an important paradigm for catalytic formation of hydrogen fuel during water reduction.27 Iron-iron and nickeliron metalorganic biomimetics imitate the structure of the enzyme active sites and also exhibit the functionality of the different hydrogenases. They demonstrate important venues for replacing the noble metal materials for the photoreduction of water.28 Water oxidation evolved as a side reaction of photosynthesis, using water as a sacrificial electron donor. Following the oxygen crisis (also known as “the Great Oxygen Event”),9,29 however, life on Earth advanced to depend on O2 as an oxidation agent for respiration and energy release from biochemical caloric substances. Currently, oxygen is the most conveniently accessible oxidant and, hence, the most widely used as such in the fossil fuel technologies. Therefore, oxidation of water to oxygen is an environmentally feasible venue for completing the electron-transfer chain in photocatalytic fuel generation. Held together by oxygen-containing bridges, that is, by O, OH, or H2O bridging moieties, calcium-manganese clusters (CaMn4OX) at the lumen side of PS II provide the catalytic activity for the four-electron oxidation of water.30,31 Although the exact structure of CaMn4OX is still debated, the development of biomimetics based on manganese-oxygen clusters proved fruitful for structural insights and for mechanistic elucidation of some of the steps in the PS II water oxidation.32 Recently, incorporation of such a polymer-embedded “fully functional” Mn4O4
Although the terms biomimetic and bioinspired are only a few decades old, biomimicry, biomimesis, and bioinspiration have been inseparable components of the technological progress through the centuries. Self-assembly at different levels provides the structural and organizational complexity of the photosynthetic apparatus essential for its energy conversion functionality. Biomimetic selfassembly of porphyrin arrays, templated by de novo designed protein helix bundles, is an important demonstration of spontaneous formation of complex structures imitating photosynthetic reaction centers (PRCs).14 Iterative tuning of the proteins and of the photoactive redox moieties of these supramolecular structures yields the desired functionality, photoinduced generation of long-range, long-lived charge-transfer states.15 Removing the protein templates from such supramolecular structures requires relatively strong bonding between the photoactive redox species to keep them in proximity with one another and to ensure the necessary electronic coupling between them. Indeed, a range of biomimetic conjugates, composed of covalently attached porphyrins, carotenes, and quinones, exhibits the desired light-harvesting functionality, that is, they mediate energy transduction and photoinduced electron transfer, leading to long-lived charge-separated states.16 Self-assembly of such synthetic triads in liposome membranes was a key demonstration of the importance of compartmentalization for photogenerating pH gradients that drive the synthesis of ATP.17 505
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Figure 2. Evolution of biomimetic into bioinspired design of molecular electrets; (a) biomimetic electret based on a protein R-helix and (b) bioinspired electret based on a polyanthranilamide. The colored arrow indicates the direction of the ground-state permanent electric dipole moment of the macromolecular electrets. The dipole originates from the ordered orientation of the amide bonds and the codirectional shift of the electron density during the formation of the hydrogen-bond network, which supports the secondary conformations of the protein and anthranilamide macromolecules. While the R-helical dipoles point from the N- to the C-termini, the anthranilamide dipoles point from the C- to the N-termini (representing the dipole direction from the positive to the negative poles).
biomimetics in dye-sensitized solar cells allowed for photocatalytic water splitting driven by illumination with visible light and without application of external potential.33 This demonstration is an important proof for the wealth of technologically relevant knowledge contained in the complexity of the biological photosynthetic systems. Due to its immense stability in the oxidizing Earth’s atmosphere, carbon dioxide readily accumulates in the air. While fluctuations in the atmospheric CO2 concentration have a grave impact on the Earth’s climate, metabolically photosynthetic organisms make an important contribution to the balance in the carbon distribution by reducing CO2 to nongaseous compounds, in which the carbon has a more negative state of oxidation than þ4. Therefore, artificial CO2 fixation will provide crucial means for balancing the recent anthropogenic increase in the atmospheric concentration of carbon dioxide.34 Adaptive and Applied Aspects of Biological Inspiration. Natural selection has given the world biomolecular systems that support a wide variety of life. As noted earlier, however, these models must be tweaked (or overhauled) to be useful in commercial energy systems. Protein helices, for example, are some of the best-known macromolecular electrets. (Electrets are materials containing electric dipoles with ordered orientation, that is, they are the electrostatic equivalent of magnets.35) Due to ordered amide and hydrogen bonds, polypeptide R-helices possess permanent dipole moments amounting to about 5 D per residue,36 resulting in an electric field exceeding 108 V m-1 in the proximity of the macromolecule (Figure 2a). These biomolecular electrets have proven immensely promising for modulating the directionality of charge transfer.23 Proteins and polypeptides, however, possess two critical disadvantages that impede their use in electronic and solar energy applications, (1) a lack of conformational stability and structural integrity when taken out of their natural environment and (2) a broad band gap (i.e., a large HOMO-LUMO energy gap) and inaccessible redox potentials that do not permit facile susceptibility to electron or hole injection.
The overall chemical and energy balance of plant photosynthesis represents the use of solar energy for conversion of water and carbon dioxide into an oxidant (oxygen) and fuel (carbohydrates), making the photosynthetic machinery an essential paradigm for developing sustainable energy technologies. Taking ideas from such biological structures for achieving permanent electric dipole moments (i.e., ordered amides held together by a network of codirectionally oriented hydrogen bonds) and incorporating them into polymeric conjugates with extended π-conjugation along their backbones yields bioinspired electrets that overcome the shortcomings of their protein counterparts (Figure 2a).37 Such synthetic molecular electrets have dipole moments of about 3-5 D per residue, thereby generating a field gradient that offsets the degeneracy of the frontier orbitals of neighboring residues and provides a cascade energy configuration for directional charge hopping.37 Furthermore, addition of electron-donating and electron-withdrawing groups to the aromatic residues of such bioinspired electrets provides a facile way to manipulate their band gaps and their redox properties, allowing for efficient electron or hole transduction.37 Biological systems provide a wide learning field for solar energy research and development. A principal shortcoming of imitative modeling after living biological systems is that they are, indeed, living. For energy to be converted from sunshine into storable chemical energy, it proceeds through a range of reactive intermediates. These reactive species inevitably are prone to 506
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The Journal of Physical Chemistry Letters damage the components of the photosynthetic apparatus.38 To survive such photodamages, the photosynthetic organisms employ (1) damage prevention by down-regulation under conditions of excessive solar radiation39 and (2) damage management by repair and restoration of damaged protein self-assemblies.40 Because the science and engineering of self-healing materials are not yet sufficiently advanced, the alternative so far has been to employ materials that have negligible susceptibility to photodamage. On the basis of the mechanistic principles of photosynthetic reaction centers, the use of light absorbers, redox couples, and charge-transport materials with pronounced photo- and electrochemical stability commenced the technology of dye-sensitized
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energy. Water oxidation and carbon dioxide fixation, for example, are two areas of solar energy research where biomimetics have the potential for an immense impact on advancing the field. The pressure to move toward bioinspiration, which seems to bring us closer to the desired technological and socioeconomic impact, may actually lead us astray if such a move is premature. Indeed, in some cases, a step backward from bioinspired to biomimetic systems may, in fact, move us forward47 by strengthening the biomimetic foundation for bioinspired technology development.
’ AUTHOR INFORMATION Corresponding Author
*E-mail:
[email protected].
A principal shortcoming of imitative modeling after living biological systems is that they are, indeed, living. solar cells41 and, later on, quantum-dot-sensitized solar cells.42,43 Platinum and conductive metal oxides have proven to be the materials of choice for electrodes carrying the hydrogen and oxygen generation, respectively, during photocatalytic water splitting. Inorganic nanostructures with defined hierarchy for photocatalytic hydrogen and oxygen production evolved from inspiration by the optical and photochemical properties of green leaves and chloroplasts.44 Despite the relative durability of the materials selected for photovoltaic and photocatalytic devices, they are still susceptible to damage and aging. Down-regulation is an important concept of light-harvesting living systems38 that, if widely adopted in the solar energy technologies, has the potential to considerably increase the lifespan of the used materials and devices. The photosynthetic down-regulation mechanisms, such as nonphotochemical quenching and state transitions,39 however, are not readily implementable in artificial light-harvesting systems. As an alternative, adopting photochromism as a regulatory mechanism, which responds to the intensity of the illumination, presents an excellent example for the adaptive capabilities of biological inspiration.45 For damage management, self-repair processes play a crucial role in the intricate sustainability of life. They involve the use of some of the stored energy for chemical repairs or replacement of damaged molecules. Technological applications of self-repair (or self-healing) promise an immense impact on the longevity of materials and devices.46,47 Although the potential of damage management for solar energy applications is still largely unexplored, key examples, such as in situ preparation and regeneration of catalytic nanostructures,48,49 point out the importance of this line of biological inspiration. What’s the Future of Biomimesis and Bioinspiration? Moving from biomimesis to bioinspiration represents the translational nature of technological development. Does such evolution in science and engineering imply that biomimetics have no future in solar energy research? No. For the past 40 years, biomimetics have proven to be an indispensible tool for testing our understanding of how living systems work. Discarding such a tool carries a streak of arrogance about our understanding of the mechanistic aspects of conversion of solar radiation into chemical
’ BIOGRAPHY Valentine Vullev received his B.Sc. from Keene State College and Ph.D. from Boston University, studying photochemistry and biophysics. As a postdoctoral fellow at Harvard University, he explored the fields of surface chemistry and microfluidics. Prof. Vullev’s current research integrates physical chemistry with biology and engineering for sustainable energy. Webpage: http://www. vullevgroup.ucr.edu ’ ACKNOWLEDGMENT The author acknowledges the National Science Foundation (CBET 0935995) for its support and Mr. Srigokul Upadhyayula, Mr. Chris Kieslich, Mr. Mitchell Boretz, and Ms. Vasilka I. Slavova for their invaluable assistance with the preparation of the figures and the cover art, and for their editing suggestions. ’ REFERENCES (1) Lewis, N. S. Toward Cost-Effective Solar Energy Use. Science 2007, 315, 798–801. (2) Barnham, K. W. J.; Mazzer, M.; Clive, B. Resolving the Energy Crisis: Nuclear or Photovoltaics? Nat. Mater. 2006, 5, 161–164. (3) Gray, H. B. Powering the Planet with Solar Fuel. Nat. Chem. 2009, 1, 7. (4) Sørensen, B. Renewable Energy: A Technical Overview. Energy Policy 1991, 19, 386–391. (5) Ciamician, G. Photochemistry of the Future. Science 1912, 36, 385–394. lectriques Produits (6) Becquerel, A.-E. Memoire Sur Les Effets E Sous L’influence Des Rayons Solaires. Comptes Rendus 1839, 9, 561– 567. (7) Monthly Energy Review; Energy Information Administration (DOE/EIA-0035): Washington, DC, June 2008. (8) Leslie, M. On the Origin of Photosynthesis. Science 2009, 323, 1286–1287. (9) Anbar, A. D.; Duan, Y.; Lyons, T. W.; Arnold, G. L.; Kendall, B.; Creaser, R. A.; Kaufman, A. J.; Gordon, G. W.; Scott, C.; Garvin, J.; Buick, R. A Whiff of Oxygen before the Great Oxidation Event? Science 2007, 317, 1903–1906. (10) Raven, J. A. Functional Evolution of Photochemical Energy Transformations in Oxygen-Producing Organisms. Funct. Plant Biol. 2009, 36, 505–515. (11) Gust, D.; Moore, T. A.; Moore, A. L. Solar Fuels Via Artificial Photosynthesis. Acc. Chem. Res. 2009, 42, 1890–1898. (12) Kupchan, S. M.; Schubert, R. M. Selective Alkylation: A Biomimetic Reaction of the Antileukemic Triptolides? Science 1974, 185, 791–793. 507
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