Crystal structures of virus-like photosystem I complexes from the mesophilic cyanobacterium Synechocystis PCC 6803

RESEARCH ARTICLE elife.elifesciences.org Crystal structures of virus-like photosystem I complexes from the mesophilic cyanobacterium Synechocystis PCC 6803 Yuval Mazor, Daniel Nataf, Hila Toporik, Nathan Nelson* Department of Biochemistry and Molecular Biology, The George S Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel Abstract Oxygenic photosynthesis supports virtually all life forms on earth. Light energy is converted by two photosystems—photosystem I (PSI) and photosystem II (PSII). Globally, nearly 50% of photosynthesis takes place in the Ocean, where single cell cyanobacteria and algae reside together with their viruses. An operon encoding PSI was identified in cyanobacterial marine viruses. We generated a PSI that mimics the salient features of the viral complex, named PSIPsaJF. PSIPsaJF is promiscuous for its electron donors and can accept electrons from respiratory cytochromes. We solved the structure of PSIPsaJF and a monomeric PSI, with subunit composition similar to the viral PSI, providing for the first time a detailed description of the reaction center and antenna system from mesophilic cyanobacteria, including red chlorophylls and cofactors of the electron transport chain. Our finding extends the understanding of PSI structure, function and evolution and suggests a unique function for the viral PSI. DOI: 10.7554/eLife.01496.001 Introduction *For correspondence: nelson@ post.tau.ac.il Competing interests: The authors declare that no competing interests exist. Funding: See page 14 Received: 09 September 2013 Accepted: 11 December 2013 Published: 28 January 2014 Reviewing editor: Werner Kühlbrandt, Max Planck Institute of Biophysics, Germany Copyright Mazor et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Oxygenic photosynthesis, which takes place in cyanobacteria, algae, and plants, provides most of the food and fuel on Earth (Barber, 2004; Nelson, 2011). Cyanobacterial photosynthetic membranes contain two photosystems, of which PSII mediates the extraction of electrons from water, the initial electron donor, to the plastoquinone pool. PSI mediates electron transfer from cytochrome C553 (or plastocyanin in eukaryotes) to ferredoxin, thereby generating the reducing power needed for CO2 fixation in the form of NADPH. The architecture of oxygenic photosynthesis in cyanobacteria has largely been determined and the structures of both photosystems from thermophilic cyanobacteria have been solved at high resolution (Jordan et al., 2001; Ferreira et al., 2004; Nelson and Ben-Shem, 2004; Amunts et al., 2007; Umena et al., 2011). Photosynthetic reaction centers are classified according to their terminal electron acceptor as either type I, with an iron sulfur cluster acceptor, or type II, with a quinone terminal acceptor. PSI, a type I reaction center, presumably evolved from the simpler homodimeric bacterial reaction centers (Buttner et al., 1992; Liebl et al., 1993; Baymann et al., 2001; Nelson and Ben-Shem, 2005). We currently know only two versions of the type I reaction centers: the relatively simple bacterial homodimer found in green sulfur bacteria (GSB), heliobacteria and Chloracidobacterium or the much more complex PSI with its 11–15 subunits found in cyanobacteria and all photosynthetic eukaryotes (Buttner et al., 1992; Hauska et al., 2001; Nelson and Yocum, 2006). Although sequence conservation between the PsaA/B subunits of PSI and the single large subunit of the homodimeric reaction centers is low, their inferred membrane topology is similar, and the sequence conservation around the bound iron sulfur cluster is high, supporting the notion of a common ancestor (Mulkidjanian and Junge, 1997; Blankenship and Hartman, 1998; Baymann et al., 2001; Mazor et al., 2012; Rutherford et al., 2012). Mazor et al. eLife 2014;3:e01496. DOI: 10.7554/eLife.01496 1 of 17 Research article Biochemistry | Biophysics and structural biology eLife digest Photosynthesis—the process by which plants and other organisms harness the energy in sunlight—is the source of almost all oxygen, food and fuel on earth. Oxygenic photosynthesis in living cells involves a series of reactions catalyzed by large protein complexes, various other soluble chemicals, and the transfer of electrons from so-called donors to acceptors. The energy in the sunlight is captured by two membrane-embedded protein complexes—photosystem I, which is the most powerful electron donor in nature, and photosystem II—and converted into chemical energy. Almost half of the world’s photosynthesis occurs in the oceans, and is performed by single-celled cyanobacteria and algae. Interestingly, some of the genes that encode photosynthetic enzymes in cyanobacteria are also found in the genomes of viruses that infect these bacteria. It is thought that these viruses can alter photosynthetic pathways in their hosts, but the interactions between these viruses and their hosts are not fully understood. Now, Mazor et al. have created a photosystem I complex that mimics the viral version of this complex, and have gone on to solve its three-dimensional structure. This mimetic virus-encoded complex was shown to be a ‘promiscuous’ electron acceptor: this means that, unlike most electron acceptors, it can accept electrons from more than one electron donor. Further, Mazor et al. solved the structure of photosystem I from Synechocystis, a cyanobacterium that lives in fresh water; and found some surprising differences between it and the only other published structure for photosystem I from a cyanobacterium (which was from a species that lives in hot water springs). These included differences in components involved in the electron transfer chain—a series of chemical reactions in which electrons are passed from donor to acceptor molecules—that were thought to be highly conserved. Other differences in the structures allowed Mazor et al. to identify the location of a unique chlorophyll pigment group in the Synechocystis photosystem I. Since Synechocystis is commonly used as a model to study photosynthesis, an improved understanding of its photosystem I should lead to further improvements in our knowledge of photosynthesis. DOI: 10.7554/eLife.01496.002 In the earth ocean’s, mainly single cell organisms, cyanobacteria or algae, perform oxygenic photosynthesis. One of the most intriguing aspects of marine cyanobacterial photosynthesis is the involvement of various viruses in the process. Hints on this involvement come from the presence of photosynthetic genes in viral genomes (Mann et al., 2003; Sullivan et al., 2006). Many marine phages encode for either the D1 gene or both D1 and D2 which together make up the reaction center of PSII (Sullivan et al., 2006). In addition, several subunits of the NDH1 complex and soluble cytochromes are also found in the viral meta (...truncated)