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

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.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.