Femtosecond optical studies of the primary charge separation reactions in far-red photosystem II from Synechococcus sp. PCC 7335
Not provided.
Biochemistry & Molecular Biology↗
Engineering topics
Shen, Gaozhong
Publications and source records attributed to Shen, Gaozhong.
Structure of the antenna complex expressed during far-red light photoacclimation in Synechococcus sp. PCC 7335
Far-red light photoacclimation, or FaRLiP, is a facultative response exhibited by some cyanobacteria that allows them to absorb and utilize lower energy light (700–800 nm) than the wavelengths typically used for oxygenic photosynthesis (400–700 nm). During this process, three essential components of the photosynthetic apparatus are altered: photosystem I, photosystem II, and the phycobilisome. In all three cases, at least some of the chromophores found in these pigment–protein complexes are replaced by chromophores that have red-shifted absorbance relative to the analogous complexes produced in visible light. Recent structural and spectroscopic studies have elucidated important features of the two photosystems when altered to absorb and utilize far-red light, but much less is understood about the modified phycobiliproteins made during FaRLiP. We used single-particle, cryo-EM to determine the molecular structure of a phycobiliprotein core complex comprising allophycocyanin variants that absorb far-red light during FaRLiP in the marine cyanobacterium Synechococcus sp. PCC 7335. The structure reveals the arrangement of the numerous red-shifted allophycocyanin variants and the probable locations of the chromophores that serve as the terminal emitters in this complex. It also suggests how energy is transferred to the photosystem II complexes produced during FaRLiP. The structure additionally allows comparisons with other previously studied allophycocyanins to gain insights into how phycocyanobilin chromophores can be tuned to absorb far-red light. These studies provide new insights into how far-red light is harvested and utilized during FaRLiP, a widespread cyanobacterial photoacclimation mechanism.
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
Two-Dimensional Electronic Spectroscopy of the Far-Red-Light Photosystem II Reaction Center
Understanding the role of specific pigments in primary energy conversion in the photosystem II (PSII) reaction center has been impeded by the spectral overlap of its constituent pigments. When grown in far-red light, some cyanobacteria incorporate chlorophyll-f and chlorophyll-d into PSII, relieving the spectral congestion. Here we employ two-dimensional electronic spectroscopy to study PSII at 77 K from Synechococcus sp. PCC 7335 cells that were grown in far-red light (FRL-PSII). We observe the formation of a radical pair within ~3 ps that we assign to Chl D1 •– P D1 •+ . While Pheo D1 is thought to act as the primary electron acceptor in PSII from cells grown in visible light, we see no evidence of its involvement, which we attribute to its reduction by dithionite treatment in our samples. Our work demonstrates that primary charge separation occurs between Chl D1 and P D1 in FRL-PSII, suggesting that P D1 /P D2 may play an underappreciated role in PSII’s charge separation mechanism.
14 SOLAR ENERGY↗
Structural comparison of allophycocyanin variants reveals the molecular basis for their spectral differences
Abstract Allophycocyanins are phycobiliproteins that absorb red light and transfer the energy to the reaction centers of oxygenic photosynthesis in cyanobacteria and red algae. Recently, it was shown that some allophycocyanins absorb far-red light and that one subset of these allophycocyanins, comprising subunits from the ApcD4 and ApcB3 subfamilies (FRL-AP), form helical nanotubes. The lowest energy absorbance maximum of the oligomeric ApcD4-ApcB3 complexes occurs at 709 nm, which is unlike allophycocyanin (AP; ApcA-ApcB) and allophycocyanin B (AP-B; ApcD-ApcB) trimers that absorb maximally at ~ 650 nm and ~ 670 nm, respectively. The molecular bases of the different spectra of AP variants are presently unclear. To address this, we structurally compared FRL-AP with AP and AP-B, performed spectroscopic analyses on FRL-AP, and leveraged computational approaches. We show that among AP variants, the α-subunit constrains pyrrole ring A of its phycocyanobilin chromophore to different extents, and the coplanarity of ring A with rings B and C sets a baseline for the absorbance maximum of the chromophore. Upon oligomerization, the α-chromophores of all AP variants exhibit a red shift of the absorbance maximum of ~ 25 to 30 nm and band narrowing. We exclude excitonic coupling in FRL-AP as the basis for this red shift and extend the results to discuss AP and AP-B. Instead, we attribute these spectral changes to a conformational alteration of pyrrole ring D, which becomes more coplanar with rings B and C upon oligomerization. This study expands the molecular understanding of light-harvesting attributes of phycobiliproteins and will aid in designing phycobiliproteins for biotechnological applications.
Gisriel, Christopher J.↗
Helical allophycocyanin nanotubes absorb far-red light in a thermophilic cyanobacterium
To compete in certain low-light environments, some cyanobacteria express a paralog of the light-harvesting phycobiliprotein, allophycocyanin (AP), that strongly absorbs far-red light (FRL). Using cryo–electron microscopy and time-resolved absorption spectroscopy, we reveal the structure-function relationship of this FRL-absorbing AP complex (FRL-AP) that is expressed during acclimation to low light and that likely associates with chlorophyll a–containing photosystem I. FRL-AP assembles as helical nanotubes rather than typical toroids due to alterations of the domain geometry within each subunit. Spectroscopic characterization suggests that FRL-AP nanotubes are somewhat inefficient antenna; however, the enhanced ability to harvest FRL when visible light is severely attenuated represents a beneficial trade-off. The results expand the known diversity of light-harvesting proteins in nature and exemplify how biological plasticity is achieved by balancing resource accessibility with efficiency.
59 BASIC BIOLOGICAL SCIENCES↗
Structure of a dimeric photosystem II complex from a cyanobacterium acclimated to far-red light
Photosystem II (PSII) is the water-splitting enzyme central to oxygenic photosynthesis. To drive water oxidation, light is harvested by accessory pigments, mostly chlorophyll (Chl) a molecules, which absorb visible light (400–700 nm). Some cyanobacteria facultatively acclimate to shaded environments by altering their photosynthetic machinery to additionally absorb far-red light (FRL, 700–800 nm), a process termed far-red light photoacclimation or FaRLiP. During far-red light photoacclimation, FRL-PSII is assembled with FRL-specific isoforms of the subunits PsbA, PsbB, PsbC, PsbD, and PsbH, and some Chl-binding sites contain Chls d or f instead of the usual Chl a. The structure of an apo-FRL-PSII monomer lacking the FRL-specific PsbH subunit has previously been determined, but visualization of the dimeric complex has remained elusive. Here, we report the cryo-EM structure of a dimeric FRL–PSII complex. The site assignments for Chls d and f are consistent with those assigned in the previous apo-FRL-PSII monomeric structure. All sites that bind Chl d or Chl f at high occupancy exhibit a FRL-specific interaction of the formyl moiety of the Chl d or Chl f with the protein environment, which in some cases involves a phenylalanine sidechain. The structure retains the FRL-specific PsbH2 subunit, which appears to alter the energetic landscape of FRL-PSII, redirecting energy transfer from the phycobiliprotein complex to a Chl f molecule bound by PsbB2 that acts as a bridge for energy transfer to the electron transfer chain. Collectively, these observations extend our previous understanding of the structure-function relationship that allows PSII to function using lower energy FRL.
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
Acclimation of the photosynthetic apparatus to low light in a thermophilic Synechococcus sp. strain
Not provided.
Plant Sciences↗
Changes in supramolecular organization of cyanobacterial thylakoid membrane complexes in response to far-red light photoacclimation
Cyanobacteria are ubiquitous in nature and have developed numerous strategies that allow them to live in a diverse range of environments. Certain cyanobacteria synthesize chlorophylls d and f to acclimate to niches enriched in far-red light (FRL) and incorporate paralogous photosynthetic proteins into their photosynthetic apparatus in a process called FRL-induced photoacclimation (FaRLiP). We characterized the macromolecular changes involved in FRL-driven photosynthesis and used atomic force microscopy to examine the supramolecular organization of photosystem I associated with FaRLiP in three cyanobacterial species. Mass spectrometry showed the changes in the proteome of Chroococcidiopsis thermalis PCC 7203 that accompany FaRLiP. Fluorescence lifetime imaging microscopy and electron microscopy reveal an altered cellular distribution of photosystem complexes and illustrate the cell-to-cell variability of the FaRLiP response.
59 BASIC BIOLOGICAL SCIENCES↗
Structure of a monomeric photosystem II core complex from a cyanobacterium acclimated to far-red light reveals the functions of chlorophylls $d$ and $f$
Far-red light (FRL) photoacclimation (FaRLiP) in cyanobacteria provides a selective growth advantage for some terrestrial cyanobacteria by expanding the range of photosynthetically active radiation to include far-red/near-infrared light (700 to 800 nm). During this photoacclimation process, photosystem II (PSII), the water:plastoquinone photooxidoreductase involved in oxygenic photosynthesis, is modified. The resulting FRL-PSII is comprised of FRL-specific core subunits and binds chlorophyll (Chl) d and Chl f molecules in place of several of the Chl a molecules found when cells are grown in visible light. These new Chls effectively lower the energy canonically thought to define the “red limit” for light required to drive photochemical catalysis of water oxidation. Changes to the architecture of FRL-PSII were previously unknown, and the positions of Chl d and Chl f molecules had only been proposed from indirect evidence. Here, we describe the 2.25-Å resolution cryo-EM structure of a monomeric FRL-PSII core complex from Synechococcus sp. PCC 7335 cells that were acclimated to FRL. We identify one Chl d molecule in the Chl D1 position of the electron transfer chain, and four Chl f molecules in the core antenna. We also make observations that enhance our understanding of PSII biogenesis, especially on the acceptor side of the complex where a bicarbonate molecule is replaced by a glutamate sidechain in the absence of the assembly factor Psb28. In conclusion, these results provide a structural basis for the lower energy limit required to drive water oxidation, which is the gateway for most solar energy utilization on Earth.
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
Structure of a photosystem I-ferredoxin complex from a marine cyanobacterium provides insights into far-red light photoacclimation
Far-red light photoacclimation (FaRLiP) exhibited by some cyanobacteria allows these organisms to use light of the far-red region of the solar spectrum (700 to 800 nm) for photosynthesis. Part of this process includes the replacement of six photosystem I (PSI) subunits with isoforms that confer the binding of chlorophyll (Chl) f molecules that are synthesized by chlorophyll f synthase and that absorb far-red light. However, the exact sites at which Chl f molecules are bound are still challenging to determine. To aid in the identification of Chl fbinding sites, we solved the cryo-EM structure of PSI from far-red light-acclimated cells (FRLPSI) of the cyanobacterium Synechococcus sp. PCC 7335. We identified six sites that bind Chl f with high specificity, and three additional sites that are likely to bind Chl f at lower specificity. All of these binding sites are in the core antenna regions of PSI, and Chl f was not observed among the electron transport cofactors. This structural analysis also reveals both conserved and non-conserved Chl f-binding sites, the latter of which exemplify the diversity in FRL-PSI among species. We found that the FRL-PSI structure also contains a bound soluble ferredoxin, PetF1, at low occupancy, which suggests that ferredoxin binds less transiently than expected according to the canonical view of ferredoxin-binding to facilitate electron transfer. We suggest that this may result from structural changes in FRL-PSI that occur specifically during FaRLiP.
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
Breaking the Red Limit: Efficient Trapping of Long-Wavelength Excitations in Chlorophyll-f-Containing Photosystem I
Not Available
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
Harvesting far-red light: Functional integration of chlorophyll f into Photosystem I complexes of Synechococcus sp. PCC 7002
Not Available
59 BASIC BIOLOGICAL SCIENCES↗
Niche expansion for phototrophic sulfur bacteria at the Proterozoic–Phanerozoic transition
Significance Carotenoid pigments afford valuable clues about the chemistry and biology of both modern and ancient aquatic environments. This study reveals that fossil aromatic carotenoids—long considered biomarkers for anoxygenic, phototrophic sulfur bacteria and their physiological requirement for hydrogen sulfide and illumination—can also be biosynthesized by oxygen-producing cyanobacteria. Cyanobacterial aromatic carotenoids, which are distinct in their chemical structures and occurrence patterns, are the most commonly encountered compounds in Proterozoic marine settings as well as in lakes from more recent eras. In contrast, carotenoids diagnostic for green sulfur bacteria of the family Chlorobiaceae became both prevalent and abundant in marine paleoenvironments beginning in the Phanerozoic Eon. This expansion occurs as marine sulfate inventories increased toward the end of the Proterozoic Eon.
59 BASIC BIOLOGICAL SCIENCES↗
The structure of Photosystem I acclimated to far-red light illuminates an ecologically important acclimation process in photosynthesis
Phototrophic organisms are superbly adapted to different light environments but often must acclimate to challenging competition for visible light wavelengths in their niches. Some cyanobacteria overcome this challenge by expressing paralogous photosynthetic proteins and by synthesizing and incorporating ~8% chlorophyll f into their Photosystem I (PSI) complexes, enabling them to grow under far-red light (FRL). We solved the structure of FRL-acclimated PSI from the cyanobacterium Fischerella thermalis PCC 7521 by single-particle, cryo–electron microscopy to understand its structural and functional differences. Four binding sites occupied by chlorophyll f are proposed. Subtle structural changes enable FRL-adapted PSI to extend light utilization for oxygenic photosynthesis to nearly 800 nm. This structure provides a platform for understanding FRL-driven photosynthesis and illustrates the robustness of adaptive and acclimation mechanisms in nature.
Science & Technology - Other Topics↗