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Oxygenic phototrophs have played a fundamental role in Earth’s history by enabling the rise of atmospheric oxygen (O₂) and paving the way for animal evolution. Understanding the origins of oxygenic photosynthesis and Cyanobacteria is key when piecing together the events around Earth’s oxygenation. It is likely that photosynthesis evolved within bacterial lineages that are not extant, so it can be challenging when studying the early history of photosynthesis. Recent genomic and molecular evolution studies have transformed our understanding about the evolution of photosynthetic reaction centres and the evolution of Cyanobacteria. The evidence reviewed here highlights some of the most recent advances on the origin of photosynthesis both at the genomic and gene family levels.

Photosynthetic reaction centres harvest the energy content of sunlight by transporting electrons across an energy-transducing biological membrane. Here we use time-resolved serial femtosecond crystallography 1 using an X-ray free-electron laser 2 to observe light-induced structural changes in the photosynthetic reaction centre of Blastochloris viridis on a timescale of picoseconds. Structural perturbations first occur at the special pair of chlorophyll molecules of the photosynthetic reaction centre that are photo-oxidized by light. Electron transfer to the menaquinone acceptor on the opposite side of the membrane induces a movement of this cofactor together with lower amplitude protein rearrangements. These observations reveal how proteins use conformational dynamics to stabilize the charge-separation steps of electron-transfer reactions. Time-resolved serial femtosecond crystallography is used to reveal the structural changes that stabilize the charge-separation steps of electron-transfer reactions in the photosynthetic reaction centre of Blastochloris viridis on a timescale of picoseconds.

Reaction centers are pigment-protein complexes that drive photosynthesis by converting light into chemical energy. It is believed that they arose once from a homodimeric protein. The symmetry of a homodimer is broken in heterodimeric reaction-center structures, such as those reported previously. The 2.2-angstrom resolution x-ray structure of the homodimeric reaction center–photosystem from the phototroph Heliobacterium modesticaldum exhibits perfect C₂ symmetry. The core polypeptide dimer and two small subunits coordinate 54 bacteriochlorophylls and 2 carotenoids that capture and transfer energy to the electron transfer chain at the center, which performs charge separation and consists of 6 (bacterio)chlorophylls and an iron-sulfur cluster; unlike other reaction centers, it lacks a bound quinone. This structure preserves characteristics of the ancestral reaction center, providing insight into the evolution of photosynthesis.

Rhodobacter ( Rba .) sphaeroides is the most widely used model organism in bacterial photosynthesis. The light-harvesting-reaction center (LH1-RC) core complex of this purple phototroph is characterized by the co-existence of monomeric and dimeric forms, the presence of the protein PufX, and approximately two carotenoids per LH1 αβ-polypeptides. Despite many efforts, structures of the Rba. sphaeroides LH1-RC have not been obtained at high resolutions. Here we report a cryo-EM structure of the monomeric LH1-RC from Rba. sphaeroides strain IL106 at 2.9 Å resolution. The LH1 complex forms a C-shaped structure composed of 14 αβ-polypeptides around the RC with a large ring opening. From the cryo-EM density map, a previously unrecognized integral membrane protein, referred to as protein-U, was identified. Protein-U has a U-shaped conformation near the LH1-ring opening and was annotated as a hypothetical protein in the Rba. sphaeroides genome. Deletion of protein-U resulted in a mutant strain that expressed a much-reduced amount of the dimeric LH1-RC, indicating an important role for protein-U in dimerization of the LH1-RC complex. PufX was located opposite protein-U on the LH1-ring opening, and both its position and conformation differed from that of previous reports of dimeric LH1-RC structures obtained at low-resolution. Twenty-six molecules of the carotenoid spheroidene arranged in two distinct configurations were resolved in the Rba. sphaeroides LH1 and were positioned within the complex to block its channels. Our findings offer an exciting new view of the core photocomplex of Rba. sphaeroides and the connections between structure and function in bacterial photocomplexes in general. Rhodobacter (Rba.) sphaeroides is a model organism for studying bacterial photosynthesis. Here, the authors present the 2.9 Å cryo-EM structure of the monomeric light-harvesting-reaction center core complex from Rba. sphaeroides strain IL106, which revealed the position and conformation of PufX and the presence of an additional component protein-U, an integral membrane protein.

The delocalized, anticorrelated component of pigment vibrations can drive nonadiabatic electronic energy transfer in photosynthetic light-harvesting antennas. In femtosecond experiments, this energy transfer mechanism leads to excitation of delocalized, anticorrelated vibrational wavepackets on the ground electronic state that exhibit not only 2D spectroscopic signatures attributed to electronic coherence and oscillatory quantum energy transport but also a cross-peak asymmetry not previously explained by theory. A number of antennas have electronic energy gaps matching a pigment vibrational frequency with a small vibrational coordinate change on electronic excitation. Such photosynthetic energy transfer steps resemble molecular internal conversion through a nested intermolecular funnel.

Understanding the mechanism behind the near-unity efficiency of primary electron transfer in reaction centers is essential for designing performance-enhanced artificial solar conversion systems to fulfill mankind’s growing demands for energy. One of the most important challenges is distinguishing electronic and vibrational coherence and establishing their respective roles during charge separation. In this work we apply two-dimensional electronic spectroscopy to three structurally-modified reaction centers from the purple bacterium Rhodobacter sphaeroides with different primary electron transfer rates. By comparing dynamics and quantum beats, we reveal that an electronic coherence with dephasing lifetime of ~190 fs connects the initial excited state, P*, and the charge-transfer intermediate P A + P B - ; this P * → P A + P B - step is associated with a long-lived quasi-resonant vibrational coherence; and another vibrational coherence is associated with stabilizing the primary photoproduct, P + B A - . The results show that both electronic and vibrational coherences are involved in primary electron transfer process and they correlate with the super-high efficiency. Distinguishing electronic and vibrational coherences helps to clarify the near-unity efficiency of primary electron transfer in reaction centres. Here, the authors report their respective correlation with the electron transfer rate by comparing the 2D electronic spectra of three mutant reaction centres.

Photosynthetic prokaryotes evolved diverse light-harvesting (LH) antennas to absorb sunlight and transfer energy to reaction centers (RC). The filamentous anoxygenic phototrophs (FAPs) are important early branching photosynthetic bacteria in understanding the origin and evolution of photosynthesis. How their photosynthetic machinery assembles for efficient energy transfer is yet to be elucidated. Here, we report the 4.1 Å structure of photosynthetic core complex from Roseiflexus castenholzii by cryo-electron microscopy. The RC–LH complex has a tetra-heme cytochrome c bound RC encompassed by an elliptical LH ring that is assembled from 15 LHαβ subunits. An N-terminal transmembrane helix of cytochrome c inserts into the LH ring, not only yielding a tightly bound cytochrome c for rapid electron transfer, but also opening a slit in the LH ring, which is further flanked by a transmembrane helix from a newly discovered subunit X. These structural features suggest an unusual quinone exchange model of prokaryotic photosynthetic machinery. Filamentous anoxygenic phototrophs (FAPs) are phylogenetically distant from other anoxygenic photosynthetic bacteria. Here the authors present the 4.1 Å cryo-EM structure of the photosynthetic core complex from the FAP Roseiflexus castenholzii and propose a model for energy and electron transfer.

Proteins are generally characterized by three-dimensional structures that are well suited for their specific function. It is much less accepted that a particular flexibility or plasticity of a protein is essential for performing its function. The latter plasticity encompasses the stochastic motions of small protein sidechains on the picosecond timescale that serve as “lubricating grease”, allowing slower functionally relevant conformational changes. Some remarkable examples of potential correlations between protein dynamics and function were observed for pigment–protein complexes in photosynthesis. For example, electron transfer and protein plasticity are concurrently suppressed in Photosystem II upon decreases in temperature or hydration, thus suggesting a prominent functional role of protein dynamics. An unusual dynamics–function correlation was observed for the major light-harvesting complex II, where the dynamics of charged protein residues affect the pigment absorption frequencies in photosynthetic light-harvesting. Generally, proteins exhibit a wide variety of motions on multiple time and length scales. However, there is an approach to characterize the plasticity of a protein as a single effective force constant that permits a straightforward comparison between different protein systems. Within this review, we determine the latter effective force constant for three photosynthetic proteins in different functional and organizational states. The force constant values determined appear to be rather different for each protein and are consistent with the requirements imposed by the various functions. These findings highlight the individual character of a protein’s flexibility and the role(s) it is playing for the specific function.

Photosynthetic electron transfers occur through multiple components ranging from small soluble proteins to large integral membrane protein complexes. Co-crystallization of a bacterial photosynthetic electron transfer complex that employs weak hydrophobic interactions was achieved by using high-molar-ratio mixtures of a soluble donor protein (high-potential iron-sulfur protein, HiPIP) with a membrane-embedded acceptor protein (reaction center, RC) at acidic pH. The structure of the co-complex offers a snapshot of a transient bioenergetic event and revealed a molecular basis for thermodynamically unfavorable interprotein electron tunneling. HiPIP binds to the surface of the tetraheme cytochrome subunit in the light-harvesting (LH1) complex-associated RC in close proximity to the low-potential heme-1 group. The binding interface between the two proteins is primarily formed by uncharged residues and is characterized by hydrophobic features. This co-crystal structure provides a model for the detailed study of long-range trans-protein electron tunneling pathways in biological systems. The high potential iron-sulfur (HiPIP) proteins are direct electron donors to the light-harvesting-reaction center complexes (LH1-RC) in photosynthetic β- and γ- Proteobacteria . Here, the authors present the 2.9 Å crystal structure of the HiPIP-bound LH1-RC complex from the thermophilic purple sulfur bacterium Thermochromatium tepidum and discuss mechanistic implications for the electron transfer pathway.

The ultra-high-resolution structure of the high-potential iron–sulfur protein at 0.48 Å, the highest-resolution X-ray crystal structure of a protein reported so far. A metalloprotein structure at 0.48 Å resolution High-resolution X-ray crystal structures of proteins feature prominently in the scientific literature, but the resolutions of these structures are rarely better than 3.0–1.5 Å. This study reports the structure of the high-potential iron–sulfur protein (HiPIP) electron carrier protein from the thermophilic purple photosynthetic bacterium Thermochromatium tepidum bacterium at 0.48 Å. This is one of the highest resolution X-ray crystal structures of a protein reported to date. The ultra-high resolution structure of this metalloprotein has enabled the authors to perform a charge-density analysis of the iron–sulfur cluster at its centre, and to visualize the distributions of valence electrons around the iron and sulphur atoms in the Fe 4 S 4 cluster. The result contributes to the understanding of the relationship between structure and function of metalloproteins at the subatomic level. The fine structures of proteins, such as the positions of hydrogen atoms, distributions of valence electrons and orientations of bound waters, are critical factors for determining the dynamic and chemical properties of proteins. Such information cannot be obtained by conventional protein X-ray analyses at 3.0–1.5 Å resolution, in which amino acids are fitted into atomically unresolved electron-density maps and refinement calculations are performed under strong restraints 1 , 2 . Therefore, we usually supplement the information on hydrogen atoms and valence electrons in proteins with pre-existing common knowledge obtained by chemistry in small molecules. However, even now, computational calculation of such information with quantum chemistry also tends to be difficult, especially for polynuclear metalloproteins 3 . Here we report a charge-density analysis of the high-potential iron–sulfur protein from the thermophilic purple bacterium Thermochromatium tepidum using X-ray data at an ultra-high resolution of 0.48 Å. Residual electron densities in the conventional refinement are assigned as valence electrons in the multipolar refinement. Iron 3 d and sulfur 3 p electron densities of the Fe 4 S 4 cluster are visualized around the atoms. Such information provides the most detailed view of the valence electrons of the metal complex in the protein. The asymmetry of the iron–sulfur cluster and the protein environment suggests the structural basis of charge storing on electron transfer. Our charge-density analysis reveals many fine features around the metal complex for the first time, and will enable further theoretical and experimental studies of metalloproteins.