Preface: special issues on photosystem II

Introduction

The appearance of oxygenic photosynthesis 3–4 billion years ago (Fournier et al. 2021) is arguably one of the most important evolutionary developments which radically transformed both the biotic and abiotic landscapes of Earth. The presence of molecular oxygen enabled the evolution of complex lifeforms requiring large amounts of chemical energy which could only be produced by aerobic respiration. Additionally, molecular oxygen remodeled the geochemistry of the planet during its transition from a reducing to an oxidizing atmosphere during the Great Oxidation Event (Bekker et al. 2004). Central to these processes is Photosystem II (PS II), the light energy-driven, water-plastoquinone oxidoreductase which initially evolved in cyanobacteria and subsequently was incorporated, along with Photosystem I (PS I), the cytochrome b₆f complex and the Ndh complex, into all algae and higher plants by the process of endosymbiosis. This membrane protein complex releases molecular oxygen and protons as the byproducts of water splitting and produces plastoquinol, which provides reducing equivalents that are used sequentially by the cytochrome b₆/f complex, PS I, and ultimately, as NADPH + H⁺, by the Calvin–Benson–Bassham cycle. Additionally, the protons released by PS II (and those pumped by the cytochrome b₆/f complex and the NDH complex (during cyclic electron transfer)) form the proton motive force that drives ATP synthesis via the ATP Synthase (Hahn et al. 2018), thus providing the chemical energy source for carbon fixation.

PS II is the most¹ studied photosynthetic membrane protein complex, with nearly 28,000 entries identified in Google Scholar over the last 10 years. These studies include numerous investigations on photon absorption, excitation energy transfer, and charge separation within the photosystem and its antenna (fsec to msec), electron transfer during oxygen evolution (msec-msec), state transitions and non-photochemical quenching (sec-min), damage and repair of the photosystem (min-hr), and adaptation to changing light environments (hr-days). PS II is truly a photosystem for all seasons, and for nearly all time scales and techniques, from 2-dimensional electronic spectroscopy to detect exciton transfer and XFEL crystal structure determinations, both in the femtosecond time domain, to the techniques of biochemistry, physiology, and cell biology (chromatography, gel electrophoresis, and gene sequencing) that require hours, or even days.

Herein, we present two Special Issues for Photosynthesis Research, entitled “Photosystem II: Structure and Function” (10 contributions) and “Photosystem II: Assembly Repair and Regulation” (12 contributions). As readers will see, the PS II time domains covered by these papers are in line with expectations for the breadth of PS II structure and activity timescales, as noted above. While these Special Issues were in the planning stages, news was received of the passing of two scientists who made substantial contributions to research on PS II, and as a result, these Special Issues are dedicated to the memories of our colleagues Professors Bridgette Barry (https://doi.org/10.1007/s11120-022-00929-4) and Ron Pace (https://doi.org/10.1007/s11120-022-00928-5) who were recently lost to the Photosynthesis Research community. Remembrances of these exceptional colleagues follow this introductory preface.

Special issue entitled photosystem II: structure and function

Consists of three review and seven research articles.

Yocum’s overview (https://doi.org/10.1007/s11120-022-00910-1) outlines the major events (development of methods for isolation of a highly active preparation, resolution and reconstitution of activity, cofactor discovery and characterization, spectroscopic analyses) that culminated in crystallization of PS II in the new millennium. The post-crystallization era has presented researchers with a number of questions, several of which are identified in this overview along with some possible answers to these remaining questions.

The review by Oliver et al. (https://doi.org/10.1007/s11120-022-00912-z) provides an in-depth look at the structure and assembly mechanism of the Mn₄CaO₅ cluster lying at the active site for water oxidation. Additionally, the authors attempt to answer the important question, “Why Manganese?” by examining the possible evolutionary origin of the manganese cluster within the context of the hypothesis that soluble Mn(II) was a primordial source of reductant for early photochemotrophic organisms.

Kato and Noguchi (https://doi.org/10.1007/s11120-021-00894-4) review the application of FTIR spectroscopy to characterization of electron transfer at the reducing side of PS II. Here, the results of experiments to analyze the Q_A⁻ /Q_B transition on the reducing side of PS II are reviewed and compared to other results on this step in PS II electron transfer.

In a slight departure from oxygenic photosynthesis, Wei et al. (https://doi.org/10.1007/s11120-022-00906-x) explore hydrogen-bonding networks surrounding Q_A and Q_B in bacterial reaction centers. As expected, Q_A is inaccessible to protons in the bulk, while Q_B is accessible via a complex network. The theoretical work aligns with earlier mutagenesis and biochemical studies to show that protons have multiple paths to Q_B. This study may act as a model for proton transfer events in PS II.

Flesher et al. (https://doi.org/10.1007/s11120-022-00911-0) report the results of computational modeling (quantum mechanics/molecular mechanics (QM/MM)) of the effects of glycerol binding in the “narrow” channel leading to the oxygen-evolving complex of PS II. The results indicate that glycerol stabilizes formation of the low-spin form (the g = 2, S = 1.2 multiline electron paramagnetic resonance (EPR) signal) associated with the S₂ state, rather than the high-spin state (g = 4.1, S = 5/2) state. These results are consistent with experimental observations obtained with PS II preparations that have been exposed to glycerol.

Gisriel and Brudvig (https://doi.org/10.1007/s11120-021-00888-2) present a structural and functional comparison of the PS II extrinsic subunits Psb27 and PsbQ. While these two proteins have similar four-helix bundle structures and binding sites on the lumenal surface of PS II, Psb27 is involved in assembly, while PsbQ is a component of mature PS II. They propose that the inherently flexible Psb27-PS II interaction may be key to efficient oxygen-evolving complex (OEC) photo-assembly.

The paper by Zhu et al. (https://doi.org/10.1007/s11120-022-00920-z) examines several residues in Thermosynechococcus vulcanus which appear to participate in the hydrogen-bonding network leading from the manganese cluster to the thylakoid lumen. Site-directed mutagenesis of the D1 residues H304, D319, N322, and R323 indicated that these residues are required for optimal oxygen evolution and stable binding of the PsbU and PsbV subunits. The authors hypothesize that these residues may also be involved in a proton egress pathway, possibly mediated by Y_Z.

Mino (https://doi.org/10.1007/s11120-022-00916-9) presents an analysis of a modified S₂ state with an EPR signal at g ~ 5 in spinach PS II membranes depleted of all extrinsic subunits in the presence of a high concentration of CaCl₂. Moving from the S₁ state to S₂ (g ~ 5) requires higher illumination temperatures than the well-studied S₂ (g = 2) or S₂ (g = 4.1) states. This result suggests that significant structural changes are required during the S₁ to S₂ (g ~ 5) transition.

Niklas et al. (https://doi.org/10.1007/s11120-022-00905-y) examine pulsed Q-band ¹H-ENDOR analyses of triplet states from both ³P680 in PS II and ³P700 in PSI. By taking measurements at each zero-field splitting canonical orientation, they produce highly accurate ¹H hyperfine coupling tensors for both photosystems’ triplet states. The data are consistent with ³P680 localized to Chl_D1 in PS II and ³P700 localized to P_A in PSI.

Patil et al. (https://doi.org/10.1007/s11120-022-00900-3) have investigated the origins of an unusual chlorophyll fluorescence response following an actinic flash in Chlamydomonas reinhardtii under microaerobic conditions. They show that when the plastoquinone pool is highly reduced and when PS II vs. PSI activity is imbalanced, Q_A⁻ can be oxidized and then re-reduced to generate a “wave phenomenon” in the chlorophyll fluorescence signal.

Special issue entitled photosystem II: assembly, repair, and regulation

Consists of one review article and eleven research articles.

Two papers examine the consequences of oxidative damage by Reactive Oxygen Species (ROS) within the photosystem. Pospíšill et al. (https://doi.org/10.1007/s11120-022-00922-x) present a review examining the role of ROS in oxidative signal transduction. The authors argue that since ROS lifetimes (and, consequently, diffusion distances) are typically short, direct retrograde signaling (chloroplast to nucleus) by ROS is unlikely. They hypothesize that oxidatively modified lipids (and possibly pigments) have longer lifetimes, and may be involved in retrograde signaling. The possibility that oxidatively modified peptides derived from the proteolysis of oxidatively damaged proteins may also be involved is also discussed. In a research article by Kale et al. (https://doi.org/10.1007/s11120-022-00902-1), differential oxidative modification, probably by ¹O₂, of Lhcb1 and Lhcb2 proteins associated with either spinach PS II membranes or PS I-LHC I-LHC II membranes was documented. The authors concluded that, in large measure, different populations of LHC II trimers were associated with PS II and PS I.

Bielczynski et al. (https://doi.org/10.1007/s11120-022-00907-w) examine the principal component of Non-Photochemical Quenching (NPQ), qE. It had been hypothesized that during the formation of qE, significant structural reorganization of the PS II supercomplex occurred which was reversed during qE relaxation (Holzwarth et al. 2009; Huang et al. 2021). Using NPQ-competent thylakoids which exhibited qE formation and relaxation, the authors demonstrated that no large structural changes occurred in the C2S2M2 and C2S2M supercomplexes.

Two papers examine manganese assimilation into the active site for water oxidation. Russell and Vinyard (https://doi.org/10.1007/s11120-021-00886-4) have used dual-mode EPR spectroscopy to study the earliest steps of photo-assembly of the PS II oxygen-evolving complex. At physiologically relevant pH values for the thylakoid lumen, they show that chloride is an essential cofactor for initial Mn(II) binding and for a deprotonation event that facilitates Mn(III) formation. Mino and Asada (https://doi.org/10.1007/s11120-021-00885-5) have identified two high affinity Mn(II) binding sites using pulsed EPR methods that shed light on the mechanism of OEC photo-assembly. Conditions were optimized to either leave one Mn(II) behind during mild depletion or to add one Mn(II) back to fully depleted samples. Their results suggest that the binding of extrinsic subunits during OEC photo-assembly changes Mn(II) binding affinity, with key implications for a proposed metal translocation model.

Two papers examine the PS II assembly factor Psb27 in cyanobacteria. Johnson et al. (https://doi.org/10.1007/s11120-021-00895-3) examine its function in Synechocystis sp. PCC 6803. These investigators examined a Psb27 deletion strain, its genetic complement, a Psb27 overexpression line, and wild type using a variety of biochemical and biophysical probes. The authors demonstrated that Psb27 elicits efficient dissipation of excitation energy preventing photodamage to pre-PS II assembly and repair complexes. Lambertz, et al. (https://doi.org/10.1007/s11120-021-00891-7), using high-resolution mass spectrometry, studied the N-terminal lipid modification of Psb27 in Thermosynechococcus elongatus BP-1. This modification is not resolved in the current cryo-EM structures of assembly complexes (Zabret et al. 2021; Knoppová et al. 2014). A total of six (!) different lipid isoforms were identified. Differential functions (if any) for these isoforms have not been determined at this time and their elucidation may provide a platform for elucidating the function(s) of N-terminal lipid modifications, in general.

Konert, et al. (https://doi.org/10.1007/s11120-022-00904-z) examined the four High-Light-Inducible proteins (Hlips) in the cyanobacterium Synechocystis sp. PCC 6803, HliA-D. These proteins are essential for survival under stress conditions. These investigators demonstrated that HliA and HliB form heterodimers with HliC. Earlier investigations (Knoppová et al. 2014) had demonstrated the heterodimeric association of HliD with HliC. The authors present a hypothesis that these heterodimers associate with the CP47 assembly module and later CP47-containing assembly intermediates, allowing the thermal dissipation of excitation energy during PS II assembly.

Rahimzadeh-Karvansara et al. (https://doi.org/10.1007/s11120-022-00908-9) introduce Psb34 as a regulatory component of PS II assembly in Synechocystis sp. PCC 6803. Psb34 binds to CP47-containing PS II intermediates competitively with high-light-inducible proteins (Hlips). A model is proposed in which Hlips bind to CP47 modules in early assembly steps and are recycled by their later replacement with Psb34.

The function of the small subunit PsbJ is explored in a work by Boussac and coworkers (https://doi.org/10.1007/s11120-021-00880-w). Using a psbJ knockout strain of Thermosynechococcus elongatus and a diverse set of biochemical and biophysical techniques, they conclude that PsbJ modulates the reduction potential of Q_B/Q_B⁻. Intriguingly, the predicted thermodynamic change would protect maturing PS II from photoinhibition and favor OEC photo-assembly.

Beckova et al. (https://doi.org/10.1007/s11120-022-00896-w) argue against the existence of a “no reaction center” intermediate of PS II assembly, which had previously been suggested (Weisz Daniel et al. 2019). This provocative work demonstrates that CP47 and CP43 intermediate modules often comigrate in native electrophoresis and ultracentrifugation experiments. By tagging either CP43 or CP47, they show that the two modules are distinct, and no combined intermediate is observed.

The paper by Havurinne et al. (https://doi.org/10.1007/s11120-021-00883-7) presents a characterization of the mechanisms by which sea slugs protect the intact plastids they acquire from Acetabularia by the process known as kleptoplasty. These fully functional intact chloroplasts are protected from photoinhibition in one of two ways according to the authors’ data. In the first way, tight packing of the plastids in the slugs occurs so that plastids in the outer layer of a cluster protect the plastids buried more deeply in the cluster. The second way utilizes screening of photoinhibitory UV light that is absorbed by the mucous and skin of the slug itself.

Conclusions

The Editors hope our readers find these papers informative and interesting. We believe that the scientific contributions contained in these two Special Issues illustrate the scope and current vitality of PS II research. We would like to thank the many authors and reviewers who made these two Special Issues possible. Additionally, thanks to Matthew Cheng, Ph.D., Associate Editor for Medicine and Life Sciences (Journals) and his support staff at Springer-Nature who make such Special Issues at Photosynthesis Research possible.