Robert E. Blankenship

Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems

Photosynthetic complexes are exquisitely tuned to capture solar light efficiently, and then transmit the excitation energy to reaction centres, where long term energy storage is initiated. The energy transfer mechanism is often described by semiclassical models that invoke ‘hopping’ of excited-state populations along discrete energy levels. Two-dimensional Fourier transform electronic spectroscopy has mapped these energy levels and their coupling in the Fenna–Matthews–Olson (FMO) bacteriochlorophyll complex, which is found in green sulphur bacteria and acts as an energy ‘wire’ connecting a large peripheral light-harvesting antenna, the chlorosome, to the reaction centre. The spectroscopic data clearly document the dependence of the dominant energy transport pathways on the spatial properties of the excited-state wavefunctions of the whole bacteriochlorophyll complex. But the intricate dynamics of quantum coherence, which has no classical analogue, was largely neglected in the analyses—even though electronic energy transfer involving oscillatory populations of donors and acceptors was first discussed more than 70 years ago, and electronic quantum beats arising from quantum coherence in photosynthetic complexes have been predicted and indirectly observed. Here we extend previous two-dimensional electronic spectroscopy investigations of the FMO bacteriochlorophyll complex, and obtain direct evidence for remarkably long-lived electronic quantum coherence playing an important part in energy transfer processes within this system. The quantum coherence manifests itself in characteristic, directly observable quantum beating signals among the excitons within the Chlorobium tepidum FMO complex at 77 K. This wavelike characteristic of the energy transfer within the photosynthetic complex can explain its extreme efficiency, in that it allows the complexes to sample vast areas of phase space to find the most efficient path.

Comparing Photosynthetic and Photovoltaic Efficiencies and Recognizing the Potential for Improvement

Comparing photosynthetic and photovoltaic efficiencies is not a simple issue. Although both processes harvest the energy in sunlight, they operate in distinctly different ways and produce different types of products: biomass or chemical fuels in the case of natural photosynthesis and nonstored electrical current in the case of photovoltaics. In order to find common ground for evaluating energy-conversion efficiency, we compare natural photosynthesis with present technologies for photovoltaic-driven electrolysis of water to produce hydrogen. Photovoltaic-driven electrolysis is the more efficient process when measured on an annual basis, yet short-term yields for photosynthetic conversion under optimal conditions come within a factor of 2 or 3 of the photovoltaic benchmark. We consider opportunities in which the frontiers of synthetic biology might be used to enhance natural photosynthesis for improved solar energy conversion efficiency.

Two-dimensional spectroscopy of electronic couplings in photosynthesis

Time-resolved optical spectroscopy is widely used to study vibrational and electronic dynamics by monitoring transient changes in excited state populations on a femtosecond timescale. Yet the fundamental cause of electronic and vibrational dynamics—the coupling between the different energy levels involved—is usually inferred only indirectly. Two-dimensional femtosecond infrared spectroscopy based on the heterodyne detection of three-pulse photon echoes has recently allowed the direct mapping of vibrational couplings, yielding transient structural information. Here we extend the approach to the visible range and directly measure electronic couplings in a molecular complex, the Fenna–Matthews–Olson photosynthetic light-harvesting protein. As in all photosynthetic systems, the conversion of light into chemical energy is driven by electronic couplings that ensure the efficient transport of energy from light-capturing antenna pigments to the reaction centre. We monitor this process as a function of time and frequency and show that excitation energy does not simply cascade stepwise down the energy ladder. We find instead distinct energy transport pathways that depend sensitively on the detailed spatial properties of the delocalized excited-state wavefunctions of the whole pigment–protein complex.

Long-lived quantum coherence in photosynthetic complexes at physiological temperature

Photosynthetic antenna complexes capture and concentrate solar radiation by transferring the excitation to the reaction center that stores energy from the photon in chemical bonds. This process occurs with near-perfect quantum efficiency. Recent experiments at cryogenic temperatures have revealed that coherent energy transfer—a wave-like transfer mechanism—occurs in many photosynthetic pigment-protein complexes. Using the Fenna–Matthews–Olson antenna complex (FMO) as a model system, theoretical studies incorporating both incoherent and coherent transfer as well as thermal dephasing predict that environmentally assisted quantum transfer efficiency peaks near physiological temperature; these studies also show that this mechanism simultaneously improves the robustness of the energy transfer process. This theory requires long-lived quantum coherence at room temperature, which never has been observed in FMO. Here we present evidence that quantum coherence survives in FMO at physiological temperature for at least 300 fs, long enough to impact biological energy transport. These data prove that the wave-like energy transfer process discovered at 77 K is directly relevant to biological function. Microscopically, we attribute this long coherence lifetime to correlated motions within the protein matrix encapsulating the chromophores, and we find that the degree of protection afforded by the protein appears constant between 77 K and 277 K. The protein shapes the energy landscape and mediates an efficient energy transfer despite thermal fluctuations.

Origin and early evolution of photosynthesis

Photosynthesis was well-established on the earth at least 3.5 thousand million years ago, and it is widely believed that these ancient organisms had similar metabolic capabilities to modern cyanobacteria. This requires that development of two photosystems and the oxygen evolution capability occurred very early in the earths history, and that a presumed phase of evolution involving non-oxygen evolving photosynthetic organisms took place even earlier. The evolutionary relationships of the reaction center complexes found in all the classes of currently existing organisms have been analyzed using sequence analysis and biophysical measurements. The results indicate that all reaction centers fall into two basic groups, those with pheophytin and a pair of quinones as early acceptors, and those with iron sulfur clusters as early acceptors. No simple linear branching evolutionary scheme can account for the distribution patterns of reaction centers in existing photosynthetic organisms, and lateral transfer of genetic information is considered as a likely possibility. Possible scenarios for the development of primitive reaction centers into the heterodimeric protein structures found in existing reaction centers and for the development of organisms with two linked photosystems are presented.

Evolution of Photosynthesis

Energy conversion of sunlight by photosynthetic organisms has changed Earth and life on it. Photosynthesis arose early in Earths history, and the earliest forms of photosynthetic life were almost certainly anoxygenic (non-oxygen evolving). The invention of oxygenic photosynthesis and the subsequent rise of atmospheric oxygen approximately 2.4 billion years ago revolutionized the energetic and enzymatic fundamentals of life. The repercussions of this revolution are manifested in novel biosynthetic pathways of photosynthetic cofactors and the modification of electron carriers, pigments, and existing and alternative modes of photosynthetic carbon fixation. The evolutionary history of photosynthetic organisms is further complicated by lateral gene transfer that involved photosynthetic components as well as by endosymbiotic events. An expanding wealth of genetic information, together with biochemical, biophysical, and physiological data, reveals a mosaic of photosynthetic features. In combination, these data provide an increasingly robust framework to formulate and evaluate hypotheses concerning the origin and evolution of photosynthesis.

THE ORIGIN AND EVOLUTION OF OXYGENIC PHOTOSYNTHESIS

The evolutionary developments that led to the ability of photosynthetic organisms to oxidize water to molecular oxygen are discussed. Two major changes from a more primitive non-oxygen-evolving reaction center are required: a charge-accumulating system and a reaction center pigment with a greater oxidizing potential. Intermediate stages are proposed in which hydrogen peroxide was oxidized by the reaction center, and an intermediate pigment, similar to chlorophyll d, was present.

Redesigning photosynthesis to sustainably meet global food and bioenergy demand

The world’s crop productivity is stagnating whereas population growth, rising affluence, and mandates for biofuels put increasing demands on agriculture. Meanwhile, demand for increasing cropland competes with equally crucial global sustainability and environmental protection needs. Addressing this looming agricultural crisis will be one of our greatest scientific challenges in the coming decades, and success will require substantial improvements at many levels. We assert that increasing the efficiency and productivity of photosynthesis in crop plants will be essential if this grand challenge is to be met. Here, we explore an array of prospective redesigns of plant systems at various scales, all aimed at increasing crop yields through improved photosynthetic efficiency and performance. Prospects range from straightforward alterations, already supported by preliminary evidence of feasibility, to substantial redesigns that are currently only conceptual, but that may be enabled by new developments in synthetic biology. Although some proposed redesigns are certain to face obstacles that will require alternate routes, the efforts should lead to new discoveries and technical advances with important impacts on the global problem of crop productivity and bioenergy production.

Niche adaptation and genome expansion in the chlorophyll d-producing cyanobacterium Acaryochloris marina

Acaryochloris marina is a unique cyanobacterium that is able to produce chlorophyll d as its primary photosynthetic pigment and thus efficiently use far-red light for photosynthesis. Acaryochloris species have been isolated from marine environments in association with other oxygenic phototrophs, which may have driven the niche-filling introduction of chlorophyll d. To investigate these unique adaptations, we have sequenced the complete genome of A. marina. The DNA content of A. marina is composed of 8.3 million base pairs, which is among the largest bacterial genomes sequenced thus far. This large array of genomic data is distributed into nine single-copy plasmids that code for >25% of the putative ORFs. Heavy duplication of genes related to DNA repair and recombination (primarily recA) and transposable elements could account for genetic mobility and genome expansion. We discuss points of interest for the biosynthesis of the unusual pigments chlorophyll d and α-carotene and genes responsible for previously studied phycobilin aggregates. Our analysis also reveals that A. marina carries a unique complement of genes for these phycobiliproteins in relation to those coding for antenna proteins related to those in Prochlorococcus species. The global replacement of major photosynthetic pigments appears to have incurred only minimal specializations in reaction center proteins to accommodate these alternate pigments. These features clearly show that the genus Acaryochloris is a fitting candidate for understanding genome expansion, gene acquisition, ecological adaptation, and photosystem modification in the cyanobacteria.

Thinking about the evolution of photosynthesis

Photosynthesis is an ancient process on Earth. Chemical evidence and recent fossil finds indicate that cyanobacteria existed 2.5–2.6 billion years (Ga) ago, and these were certainly preceded by a variety of forms of anoxygenic photosynthetic bacteria. Carbon isotope data suggest autotrophic carbon fixation was taking place at least a billion years earlier. However, the nature of the earliest photosynthetic organisms is not well understood. The major elements of the photosynthetic apparatus are the reaction centers, antenna complexes, electron transfer complexes and carbon fixation machinery. These parts almost certainly have not had the same evolutionary history in all organisms, so that the photosynthetic apparatus is best viewed as a mosaic made up of a number of substructures each with its own unique evolutionary history. There are two schools of thought concerning the origin of reaction centers and photosynthesis. One school pictures the evolution of reaction centers beginning in the prebiotic phase while the other school sees reaction centers evolving later from cytochrome b in bacteria. Two models have been put forth for the subsequent evolution of reaction centers in proteobacteria, green filamentous (non-sulfur) bacteria, cyanobacteria, heliobacteria and green sulfur bacteria. In the selective loss model the most recent common ancestor of all subsequent photosynthetic systems is postulated to have contained both RC1 and RC2. The evolution of reaction centers in proteobacteria and green filamentous bacteria resulted from the loss of RC1, while the evolution of reaction centers in heliobacteria and green sulfur bacteria resulted from the loss of RC2. Both RC1 and RC2 were retained in the cyanobacteria. In the fusion model the most recent common ancestor is postulated to have given rise to two lines, one containing RC1 and the other containing RC2. The RC1 line gave rise to the reaction centers of heliobacteria and green sulfur bacteria, and the RC2 line led to the reaction centers of proteobacteria and green filamentous bacteria. The two reaction centers of cyanobacteria were the result of a genetic fusion of an organism containing RC1 and an organism containing RC2. The evolutionary histories of the various classes of antenna/light-harvesting complexes appear to be completely independent. The transition from anoxygenic to oxygenic photosynthesis took place when the cyanobacteria learned how to use water as an electron donor for carbon dioxide reduction. Before that time hydrogen peroxide may have served as a transitional donor, and before that, ferrous iron may have been the original source of reducing power.