Structural and Functional Dynamics of Photosynthetic Antenna Complexes
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COMMENTARY COMMENTARY Structural and functional dynamics of photosynthetic antenna complexes Robert E. Blankenship1 begin the long series of processes that lead Departments of Biology and Chemistry, Washington University in St. Louis, St. Louis, to long-term energy storage in the form of MO 63130 biomass (2). In many cases, these antenna complexes can be purified away from the Photosynthetic organisms face a special chal- organisms, which contain two coupled light- reaction centers and their light-absorbing lenge. They must absorb large numbers of driven reaction centers that must coordinate and regulatory properties can be studied solar photons to provide the energy to power electron flow despite significantly different in molecular detail. In PNAS, Wang and their metabolism, yet too much energy can be kinetic and spectral properties. The job of Moerner (3) have carried out an in-depth extremely damaging and can lead to rapid collecting photons, efficiently distributing analysis of a photosynthetic antenna com- cell death (1). Maintaining the balance be- the energy to the place where it is needed, plex, the allophycocyanin pigment protein found as part of the larger phycobilisome tween too little and too much energy, espe- and protecting the organism against photo- complex in cyanobacteria, revealing in re- cially in the face of light intensity fluctuations damage falls to the photosynthetic antenna markable detail the complexities of the en- that can change by orders of magnitude system. These antenna systems are special- ergy transfer and photodegradation processes within milliseconds, requires a sophisticated ized for the absorption of photons and that take place. system that has multiple levels of regulation transfer of energy in the form of excited Phycobilisomes are large peripheral mem- and repair. The challenge is especially states or excitons to the photosynthetic re- brane pigment–protein complexes that are complex for oxygen-evolving photosynthetic action center, where electron transfer processes attached to the cytoplasmic side of the thyla- koid membrane that contains the reaction centers (4–9). They are made up of several types of pigment-containing proteins, whose pigments are covalently attached open-chain tetrapyrrole pigments called bilins. Phycobi- lisomes also contain numerous colorless pro- teins collectively known as linkers, which help to organize the system and also fine- tune the spectral properties of the pigment- containing subunits to direct the energy flow to the reaction centers, which are integral membrane complexes that contain chloro- phylls and other electron transfer cofactors. Theentirephycobilisomecomplexcanhave a mass of several million daltons. Phycobili- somes have been known for many years to transfer energy mainly to photosystem II, the water-oxidizing photosystem, or, in some cases, to photosystem I (10). Recently, it has been shown that a “megacomplex” containing both photosystems and the phycobilisome is present (11). Fig. 1 shows a structural model that incorporates structural features of phyco- biliproteins and reaction centers and their spatial relationships. The phycobiliproteins are organized into rods that feed energy into a central core structure, which then rapidly Fig. 1. Structural model of a phycobilisome antenna complex associated with both photosystem I and photosystem and efficiently transfers excitations to the II in a megacomplex. The model is based on X-ray crystal structures of the phycocyanin and allophycocyanin proteins reaction centers in the membrane. and the reaction centers. The relative positions and orientations of the phycobilisome and reaction centers are based on chemical cross-linking and MS studies (11). Color coding is as follows: phycocyanin, blue; allophycocyanin, orange; reaction centers are shown in red (negative charged residues), blue (positively charged residues), and tan (uncharged residues). Author contributions: R.E.B. wrote the paper. Photosystem II is present as a dimeric complex directly under the core of the phycobilisome, with the downward-pointing The author declares no conflict of interest. lobes that make up the accessory subunits of the oxygen-evolving system. Photosystem I is present as two copies of a trimeric complex that flanks the central attachment site of the phycobilisome on photosystem II. The lipids of the thylakoid See companion article on page 13880. membrane bilayer are shown in green. Image courtesy of Haijun Liu (Washington University in St. Louis, St. Louis). 1Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1519063112 PNAS | November 10, 2015 | vol. 112 | no. 45 | 13751–13752 Downloaded by guest on September 28, 2021 The pathway of energy transfer in phyco- that the orange carotenoid protein binds to shared the 2014 Nobel Prize in Chemistry. bilisomes has been established to be direc- the allophycocyanin near where pigment beta They trapped both monomeric and trimeric tional along the rods, which are sometimes resides. The quenching is proposed to take complexes of allophycocyanin in an electro- “ ” described as light guides (5). The allophy- place by Förster resonance energy transfer kinetic trap that cancels diffusion and then cocyanin complex studied in detail by Wang from the bilin pigment to the nearby carot- examined them in detail in terms of stability and Moerner (3) is intermediate in the en- enoid, which then safely dissipates the energy and spectral properties. Perhaps the most ergy transfer system, receiving excitations surprising aspect of the results reported by from the phycocyanin complexes that make Wang and Moerner Wang and Moerner (3) is that the two pig- up the rods and transferring them to the have carried out an terminal emitter complexes that, in turn, feed ments in each alpha/beta monomer subunit, the reaction centers. in-depth analysis of a although chemically identical, have signifi- The basic architecture of the components photosynthetic cantly different properties, particularly their of the phycobilisome is a trimeric building antenna complex, the susceptibility to photodegradation. The tri- block. Each “monomer” subunit in the tri- mers, which have six bilin pigments, show meric complex consists of a heterodimeric allophycocyanin even more complex behavior with a number protein complex containing an alpha and pigment protein found of distinct states that depend on the level of beta protein chain. Each of the protein chains as part of the larger intactness of the complex during photo- has one to three covalently attached bilin bleaching. Their work provides an unprece- pigments, depending on the type of phycobi- phycobilisome complex dented level of molecular detail of the inner liprotein. In the allophycocyanin complex in cyanobacteria. workings of the phycobilisome antenna considered here, there are a total of six pig- complex and electronic properties of the ments in the trimeric assembly. These tri- as heat (13). The orange carotenoid protein pigments in their natural environment. It meric complexes then further assemble into undergoes a substantial conformational hexameric discs, and several of the discs form change upon the transition from the non- thus provides a solid foundation to under- the core structure of the phycobilisome, along quenching orange form to the quenching red stand the larger scale processes that take with some additional subunits that facilitate form, which is thought to position the ca- place in the complete phycobilisome, in- the energy transfer to the reaction center. The rotenoid more favorably to quench excita- cluding its regulation. – phycocyanin subunits have a similar overall tions in the bound form (14 16). The study of Wang and Moerner (3) uses ACKNOWLEDGMENTS. This work was supported by architecture but contain three bilin pigments Grant DE-FG02-07ER15902 from the Photosynthetic Sys- per trimer. The hexameric discs of phycocy- the single molecule spectroscopy technique, tems Program of the US Department of Energy, Office of anin form the extended rods in the phycobi- which Moerner pioneered and for which he Science, Basic Energy Sciences. lisome. In some species of cyanobacteria, a third type of phycobiliprotein called phyco- 1 Blankenship RE (2014) Molecular Mechanisms of Photosynthesis 10 Mullineaux CW (2008) Phycobilisome-reaction centre interaction erythrin is found at the tips of the rods. (Wiley–Blackwell, Oxford), 2nd Ed. in cyanobacteria. Photosynth Res 95(2-3):175–182. 2 Croce R, van Amerongen H (2014) Natural strategies for 11 Liu H, et al. (2013) Phycobilisomes supply excitations to both The allophycocyanin complex is also photosynthetic light harvesting. Nat Chem Biol 10(7):492–501. photosystems in a megacomplex in cyanobacteria. Science thought to be the site of action of the major 3 Wang Q, Moerner WE (2015) Dissecting pigment architecture of 342(6162):1104–1107. regulatory process in phycobilisomes, en- individual photosynthetic antenna complexes in solution. Proc Natl 12 Kirilovsky D (2015) Modulating energy arriving at photochemical Acad Sci USA 112:13880–13885. reaction centers: Orange carotenoid protein-related photoprotection ergy quenching that is mediated by a water- 4 Gantt E, Conti SF (1966) Phycobiliprotein localization in algae. and state transitions. Photosynth Res 126(1):3–17. solubleorangecarotenoidprotein(12). Brookhaven Symp Biol 19:393–405. 13 Zhang H, et al. (2014) Molecular mechanism of photoactivation This protein has a photocycle in which, 5 Glazer AN (1985) Light harvesting by phycobilisomes.