Photosynthetic antenna complexes capture and concentrate solar radiation by transferring the excitation to the reaction center that stores energy from the photon in chemical bonds. This process occurs with near-perfect quantum efficiency. Recent experiments at cryogenic temperatures have revealed that coherent energy transfer-a wave-like transfer mechanism-occurs in many photosynthetic pigment-protein complexes. Using the Fenna-MatthewsOlson antenna complex (FMO) as a model system, theoretical studies incorporating both incoherent and coherent transfer as well as thermal dephasing predict that environmentally assisted quantum transfer efficiency peaks near physiological temperature; these studies also show that this mechanism simultaneously improves the robustness of the energy transfer process. This theory requires long-lived quantum coherence at room temperature, which never has been observed in FMO. Here we present evidence that quantum coherence survives in FMO at physiological temperature for at least 300 fs, long enough to impact biological energy transport. These data prove that the wave-like energy transfer process discovered at 77 K is directly relevant to biological function. Microscopically, we attribute this long coherence lifetime to correlated motions within the protein matrix encapsulating the chromophores, and we find that the degree of protection afforded by the protein appears constant between 77 K and 277 K. The protein shapes the energy landscape and mediates an efficient energy transfer despite thermal fluctuations.biophysics | photosynthesis | quantum beating | ultrafast spectroscopy | quantum biology E nergy transfer through photosynthetic pigment-protein complexes operates with exceptionally high quantum efficiency (1). Recent studies have demonstrated that energy moves through antennae using not only a classical hopping mechanism but also a manifestly quantum mechanical wave-like mechanism at cryogenic temperatures (2-5). Theoretical studies of this process within the Fenna-Matthews-Olson antenna complex (FMO) show that this quantum transport mechanism requires a balance between unitary (oscillatory) and dissipative (dephasing) dynamics; further, this balance appears to be optimized near room temperature and contributes to the robustness of the process (6-9). This theory demands that quantum coherence persist long enough to affect transport, but quantum beating has never been observed in FMO at physiological temperature.The FMO pigment-protein complex from Chlorobium tepidum serves as a model system for photosynthetic energy transfer processes (2, 10-13). This complex conducts energy from the larger light-harvesting chlorosome to the reaction center in green sulfur bacteria (14, 15). Each noninteracting FMO monomer contains seven coupled bacteriochlorophyll-a chromophores arranged asymmetrically, yielding seven nondegenerate, delocalized molecular excited states called excitons (11,16). The small number of distinct states makes this particular complex attractive for theoretical studies o...

Protein phosphorylation is a fundamental mechanism regulating nearly every aspect of cellular life. Several secreted proteins are phosphorylated, but the kinases responsible are unknown. We identified a family of atypical protein kinases that localize within the Golgi apparatus and are secreted. Fam20C appears to be the Golgi casein kinase that phosphorylates secretory pathway proteins within S-x-E motifs. Fam20C phosphorylates the caseins and several secreted proteins implicated in biomineralization, including the small integrin-binding ligand, N-linked glycoproteins (SIBLINGs). Consequently, mutations in Fam20C cause an osteosclerotic bone dysplasia in humans known as Raine syndrome. Fam20C is thus a protein kinase dedicated to the phosphorylation of extracellular proteins.

The absorbance spectrum of the Fenna-Matthews-Olson protein--a component of the antenna system of Green Sulfur Bacteria--is always one of two types, depending on the species of the source organism. The FMO from Prosthecochloris aestuarii 2K has a spectrum of type 1 while that from Chlorobaculum tepidum is of type 2. The previously reported crystal structures for these two proteins did not disclose any rationale that would explain their spectral differences. We have collected a 1.3 A X-ray diffraction dataset of the FMO from Prosthecochloris aestuarii 2K, which has allowed us to identify an additional Bacteriochlorophyll-a molecule with chemical attachments to both sides of the central magnesium atom. A new analysis of the previously published X-ray data for the Chlorobaculum tepidum FMO shows the presence of a Bacteriochlorophyll-a molecule in an equivalent location but with a chemical attachment from only one side. This difference in binding is shown to be predictive of the spectral type of the FMO.

Summary The existence of extracellular phosphoproteins has been acknowledged for over a century. However, research in this area has been undeveloped largely because the kinases that phosphorylate secreted proteins have escaped identification. Fam20C is a kinase that phosphorylates S-x-E/pS motifs on proteins in milk and in the extracellular matrix of bones and teeth. Here, we show that Fam20C generates the majority of the extracellular phosphoproteome. Using CRISPR/Cas9 genome editing, mass spectrometry, and biochemistry, we identify more than 100 secreted phosphoproteins as genuine Fam20C substrates. Further, we show that Fam20C exhibits broader substrate specificity than previously appreciated. Functional annotations of Fam20C substrates suggest roles for the kinase beyond biomineralization, including lipid homeostasis, wound healing, and cell migration and adhesion. Our results establish Fam20C as the major secretory pathway protein kinase and serve as a foundation for new areas of investigation into the role of secreted protein phosphorylation in human biology and disease.

The high excitation energy-transfer efficiency demanded in photosynthetic organisms relies on the optimal pigment-protein binding orientation in the individual protein complexes and also on the overall architecture of the photosystem. In green sulfur bacteria, the membrane-attached Fenna-Matthews-Olson (FMO) antenna protein functions as a ''wire'' to connect the large peripheral chlorosome antenna complex with the reaction center (RC), which is embedded in the cytoplasmic membrane (CM). Energy collected by the chlorosome is funneled through the FMO to the RC. Although there has been considerable effort to understand the relationships between structure and function of the individual isolated complexes, the specific architecture for in vivo interactions of the FMO protein, the CM, and the chlorosome, ensuring highly efficient energy transfer, is still not established experimentally. Here, we describe a mass spectrometrybased method that probes solvent-exposed surfaces of the FMO by labeling solvent-exposed aspartic and glutamic acid residues. The locations and extents of labeling of FMO on the native membrane in comparison with it alone and on a chlorosome-depleted membrane reveal the orientation. The large differences in the modification of certain peptides show that the Bchl a #3 side of the FMO trimer interacts with the CM, which is consistent with recent theoretical predictions. Moreover, the results also provide direct experimental evidence to confirm the overall architecture of the photosystem from Chlorobaculum tepidum (C. tepidum) and give information on the packing of the FMO protein in its native environment.chemical labeling ͉ energy transfer ͉ FMO protein ͉ mass spectrometry ͉ protein footprinting P hotosynthesis is a fundamental biological process that harvests solar energy to power life on Earth (1). A diverse family of pigment-protein complexes and elegant architectures accomplish the necessary light-harvesting and energy-storage processes (2-5). In photosynthetic green sulfur bacteria, light absorbed by a large antenna complex known as a chlorosome (6-8) is transferred through a protein called Fenna-Matthews-Olson (FMO) (9) to the reaction center, which is embedded in the cytoplasmic membrane (CM). Together, they form a funnel-like architecture to facilitate energy transfer. The specific orientation of the critical linker, the FMO protein, however is unknown (Fig. 1A).The structure of the FMO protein was the first (bacterio)chlorophyll binding protein to be determined by X-ray crystallography. Structures of this protein from 2 species, Prosthecochloris aestuarii 2K (10, 11) and Chlorobaculum tepidum (12) are now available, and they show strong structural and spectral similarities. The FMO protein consists of 3 identical subunits of mass 40 kDa related by a 3-fold axis of symmetry. The 3 monomers form a disc with a C3 symmetry axis perpendicular to the disc plane (Fig. 1B). There are 7 BChl a molecules in a monomer, although an eighth pigment has been resolved in newly solved structures (13,14). Eac...