Christiaan Sybesma (August 31, 1928-January 31, 2018), an extraordinary biophysicist of our time.

We provide here a brief Tribute to Christiaan Sybesma (1928-2018), a highly respected biophysicist of our time. We remember him by giving a brief highlight of his life and a glimpse of his outstanding contributions in photosynthesis. He was a charming and highly respected scientist of our time.

Nature does not rely on long-lived electronic quantum coherence for photosynthetic energy transfer.

During the first steps of photosynthesis, the energy of impinging solar photons is transformed into electronic excitation energy of the light-harvesting biomolecular complexes. The subsequent energy transfer to the reaction center is commonly rationalized in terms of excitons moving on a grid of biomolecular chromophores on typical timescales [Formula: see text]100 fs. Today's understanding of the energy transfer includes the fact that the excitons are delocalized over a few neighboring sites, but the role of quantum coherence is considered as irrelevant for the transfer dynamics because it typically decays within a few tens of femtoseconds. This orthodox picture of incoherent energy transfer between clusters of a few pigments sharing delocalized excitons has been challenged by ultrafast optical spectroscopy experiments with the Fenna-Matthews-Olson protein, in which interference oscillatory signals up to 1.5 ps were reported and interpreted as direct evidence of exceptionally long-lived electronic quantum coherence. Here, we show that the optical 2D photon echo spectra of this complex at ambient temperature in aqueous solution do not provide evidence of any long-lived electronic quantum coherence, but confirm the orthodox view of rapidly decaying electronic quantum coherence on a timescale of 60 fs. Our results can be considered as generic and give no hint that electronic quantum coherence plays any biofunctional role in real photoactive biomolecular complexes. Because in this structurally well-defined protein the distances between bacteriochlorophylls are comparable to those of other light-harvesting complexes, we anticipate that this finding is general and directly applies to even larger photoactive biomolecular complexes.

Evidence for a cysteine-mediated mechanism of excitation energy regulation in a photosynthetic antenna complex.

Light-harvesting antenna complexes not only aid in the capture of solar energy for photosynthesis, but regulate the quantity of transferred energy as well. Light-harvesting regulation is important for protecting reaction center complexes from overexcitation, generation of reactive oxygen species, and metabolic overload. Usually, this regulation is controlled by the association of light-harvesting antennas with accessory quenchers such as carotenoids. One antenna complex, the Fenna-Matthews-Olson (FMO) antenna protein from green sulfur bacteria, completely lacks carotenoids and other known accessory quenchers. Nonetheless, the FMO protein is able to quench energy transfer in aerobic conditions effectively, indicating a previously unidentified type of regulatory mechanism. Through de novo sequencing MS, chemical modification, and mutagenesis, we have pinpointed the source of the quenching action to cysteine residues (Cys49 and Cys353) situated near two low-energy bacteriochlorophylls in the FMO protein from Chlorobaculum tepidum Removal of these cysteines (particularly removal of the completely conserved Cys353) through N-ethylmaleimide modification or mutagenesis to alanine abolishes the aerobic quenching effect. Electrochemical analysis and electron paramagnetic resonance spectra suggest that in aerobic conditions the cysteine thiols are converted to thiyl radicals which then are capable of quenching bacteriochlorophyll excited states through electron transfer photochemistry. This simple mechanism has implications for the design of bio-inspired light-harvesting antennas and the redesign of natural photosynthetic systems.

Remembering John M. Olson (1929-2017).

Here we provide reflections of and a tribute to John M. Olson, a pioneering researcher in photosynthesis. We trace his career, which began at Wesleyan University and the University of Pennsylvania, and continued at Utrech in The Netherlands, Brookhaven National Laboratory, and Odense University in Denmark. He was the world expert on pigment organization in the green photosynthetic bacteria, and discovered and characterized the first chlorophyll-containing protein, which has come to be known as the Fenna-Matthews-Olson (FMO) protein. He also thought and wrote extensively on the origin and early evolution of photosynthesis. We include personal comments from Brian Matthews, Raymond Cox, Paolo Gerola, Beverly Pierson and Jon Olson.

Contribution of bacteriochlorophyll conformation to the distribution of site-energies in the FMO protein.

The structural data for the Fenna-Matthews-Olson (FMO) protein indicate that the bacteriochlorophylls (BChls) display a significant degree of conformational heterogeneity of their peripheral substituents and the protein-induced nonplanar skeletal deformations of the tetrapyrrole macrocycle. As electronic properties of chromophores are altered by such differences, a conformational effect may influence the site-energies of specific pigments and thus play a role in mediating the excitation energy transfer dynamics, but this has not yet been established. The difficulty of assessing this question is shown to be partly the result of the inability of the sequential truncation approach usually employed to account for interactions between the conformations of the macrocycle and its substituents and an alternative approach is suggested. By assigning the BChl atoms to meaningful atom groups and performing all possible permutations of partial optimizations in a full-factorial design, where each group is either frozen in the crystal geometry or optimized in vacuo, followed by excited state calculations on each resulting structure (PM6//ZIndo/S), the specific effects of the conformations of each BChl component as well as mutual interactions between the molecular fragments on the site-energy can be delineated. This factorial relaxation procedure gives different estimates of the macrocycle conformational perturbation than the approach of sequentially truncating the BChl periphery. The results were evaluated in the context of published site-energies for the FMO pigments from three species to identify how conformational effects contribute to their distribution and instances of cross-species conservation and functional divergence of the BChl nonplanarity conformational contribution are described.

Native FMO-reaction center supercomplex in green sulfur bacteria: an electron microscopy study.

Chlorobaculum tepidum is a representative of green sulfur bacteria, a group of anoxygenic photoautotrophs that employ chlorosomes as the main light-harvesting structures. Chlorosomes are coupled to a ferredoxin-reducing reaction center by means of the Fenna-Matthews-Olson (FMO) protein. While the biochemical properties and physical functioning of all the individual components of this photosynthetic machinery are quite well understood, the native architecture of the photosynthetic supercomplexes is not. Here we report observations of membrane-bound FMO and the analysis of the respective FMO-reaction center complex. We propose the existence of a supercomplex formed by two reaction centers and four FMO trimers based on the single-particle analysis of the complexes attached to native membrane. Moreover, the structure of the photosynthetic unit comprising the chlorosome with the associated pool of RC-FMO supercomplexes is proposed.

Neutron and X-ray analysis of the Fenna-Matthews-Olson photosynthetic antenna complex from Prosthecochloris aestuarii.

The Fenna-Matthews-Olson protein from Prosthecochloris aestuarii (PaFMO) has been crystallized in a new form that is amenable to high-resolution X-ray and neutron analysis. The crystals belonged to space group H3, with unit-cell parameters a = b = 83.64, c = 294.78 Å, and diffracted X-rays to ∼1.7 Šresolution at room temperature. Large PaFMO crystals grown to volumes of 0.3-0.5 mm3 diffracted neutrons to 2.2 Šresolution on the MaNDi neutron diffractometer at the Spallation Neutron Source. The resolution of the neutron data will allow direct determination of the positions of H atoms in the structure, which are believed to be fundamentally important in tuning the individual excitation energies of bacteriochlorophylls in this archetypal photosynthetic antenna complex. This is one of the largest unit-cell systems yet studied using neutron diffraction, and will allow the first high-resolution neutron analysis of a photosynthetic antenna complex.