Structure-function relationships in photosynthetic membranes: Challenges and emerging fields

Accepted Manuscript Title: Structure-function relationships in photosynthetic membranes: Challenges and Emerging Fields Author: Helmut Kirchhoff PII: DOI: Reference:

S0168-9452(17)30607-6 https://doi.org/10.1016/j.plantsci.2017.09.021 PSL 9686

To appear in:

Plant Science

Received date: Revised date: Accepted date:

7-7-2017 26-9-2017 29-9-2017

Please cite this article as: Helmut Kirchhoff, Structure-function relationships in photosynthetic membranes: Challenges and Emerging Fields, Plant Science https://doi.org/10.1016/j.plantsci.2017.09.021 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Review: Structure-function relationships in photosynthetic membranes: Challenges and Emerging Fields Helmut Kirchhoff Institute of Biological Chemistry, Washington State University, PO Box 646340, Pullman, 99164, WA, USA

Highlights: 

The structure of photosynthetic membranes is highly responsive to environmental conditions, constantly changing their shape.

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Switching the supramolecular arrangement of photosystem II from a disordered to semicrystalline state control lateral diffusion and light harvesting in thylakoid membranes.

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Dynamic changes in physicochemical properties of the lipid bilayer can control the conformation and supramolecular organization of proteins in photosynthetic membranes.

Abstract Oxygenic photosynthesis is a fundamental biological process that shaped the earth’s biosphere. The process of energy transformation is hosted in highly specialized thylakoid membranes that adjust their architecture in response to environmental cues at different structural levels leading to the adjustment of photosynthetic functions. This review presents structure-function dynamics ranging from the whole membrane system over the mesoscopic level (protein ensembles) down

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to interactions between lipids and protein complexes. On the whole membrane level, thylakoid membranes constantly change their overall shape (e.g. membranes swell and shrink or destack and stack) that controls vital functions of energy transformation. Furthermore, the physical connection and transition between stacked grana thylakoid and unstacked membrane regions that determines mass transport between these sub-compartments is a crucial open question. On the mesoscopic level, it turns out that reorganizations between disordered and ordered protein arrangements is central for light harvesting and lateral diffusion processes. It has to be unraveled how changes in mesoscopic protein organization are controlled. Finally, dynamic physicochemical properties of the lipid bilayer can determine the structure and organization of photosynthetic membrane proteins, a field that is highly neglected so far. This review focusses on open questions and challenging problems in photosynthesis research.

Oxygenic photosynthesis The advent of oxygenic photosynthesis, dated between 2.9 to 2.4 billion years ago, was a key step in the evolution of life on earth and strongly shaped and still shapes the geochemistry and biosphere of our planet (1). The water-splitting by photosystem II (PSII) that gives access to a virtually infinite reservoir of electron donors, the wiring of two photosystems in series, the optimized pigment packing in light harvesting complexes (LHC), the generation of a proton motive force (pmf) by proton-pumping electron transport complexes, and the coupling of ATP formation with the relative rotation between the Fo and F1 parts of the mechanochemical ATPase are just a few examples for the inventive power of evolution leading to a highly efficient and robust energy converting photosynthetic apparatus. Consequently, today, oxygenic

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phototrophs are distributed over many different taxonomic groups including cyanobacteria, diatoms, red and green algae, mosses, and higher plants that are ubiquitously spread over our planet (2). Over the last three decades, our knowledge about the structure and function of photosynthetic machineries reached a point that allows detailed insights in how energy conversion works from a sub-molecular to the whole membrane level. This makes photosynthetic membranes one of the best-characterized biomembranes with huge promises to optimize and conduct energy conversion for special and urgent needs of mankind. The aim of this review is not to survey this scientific progress but rather to identify critical gaps in our knowledge base and offer potential ways to fill these gaps. This review will start with the overall organization of photosynthetic membranes, zooming into the mesocopic level characterized by the organization of many photosynthetic protein complexes and finally reaching the molecular level. In this way, length scales ranging from micrometers to nanometers will be covered. The focus will be on thylakoid membranes of higher plants but other clades will be addressed as well.

Structural organization of photosynthetic membranes – the micrometer length scale A. Higher Plants Over many decades, electron microscopy on ultrathin-sectioned material was the main technique to study, in detail, the overall thylakoid membrane organization (reviewed in 3). Based on these ‘classical’ EM techniques, reconstitution of the complex 3D thylakoid structure was possible from serial thin sections (see for example 4). This was a tedious and difficult task but it led to sophisticated 3D models of thylakoid membranes. In the last decade, however, the situation changed significantly by technical breakthroughs in electron tomography (ET) that now allows high-resolution spatial visualization of the overall membrane architecture (5-8). Today, cryo-ET

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is a highly active research field with the trend to resolve individual protein supercomplexes at 7 nm resolution and higher in intact cells and tissues, for example sub-tomogram averaging (7, 9, 10). A crucial technical requirement for the application of cryo-ET is a high-quality of flashfrozen sections of not more than several hundred nanometer thickness. In this respect, focused ion beam (FIB) milling on cryo-fixed samples offers promising possibilities (11). ET image analyses largely confirm older models of higher plant thylakoid membranes showing cylindrical stacked membranes of 350-600 nm in diameter, so-called grana thylakoids interconnected by unstacked stroma lamellae, forming a continuous complex structured membrane network that separates the aqueous thylakoid lumen from the stroma (higher plants and algae). In cyanobacteria, the thylakoid membrane separates the lumen from the cytoplasm. Although the different ET studies agree on the overall thylakoid structure, an important detail has been highly debated. This detail centers around the question of how stroma lamellae connect into grana membranes at the periphery of the grana cylinder (reviewed in 12, 13). In the ‘helical fretwork’ model, stroma lamellae wind around the grana cylinder in the form of a right-handed helix and inserts into the grana cylinder via small slits called ‘frets’. In contrast, the ‘bifurcation’ model that is based on the original ‘fork’ model (14) proposes that stroma membranes split into two membranes (bifurcation) that then form the grana stacks. In addition, the bifurcation model postulates that adjacent grana membranes can form membrane bridges to connect directly to each other (13). The physiological importance of the exact geometry of the junction between grana and stroma thylakoid membranes is that it determines the exchange for proteins and metabolites between stacked and unstacked regions. Electron transport processes (diffusion of plastoquinone and plastocyanin), regulation for light harvesting (redistribution of LHCII by state transition), or the repair of photodamage PSII are all examples of processes that require brisk traffic between

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stacked grana and unstacked thylakoid membrane regions. The wider the connection zones between grana membranes and stroma lamellae the faster mass transport between these thylakoid subdomains both within the membrane and in the thylakoid lumen. Thus, the architecture of the grana cylinder-stroma lamellae transition is an important gatekeeper for transport processes. Due to fast improvements in cryo-ET, it is likely that new ultrastructural in situ data with superb image quality will resolve the controversy between the ‘helical fretwork’ and the ‘bifurcation’ model in the near future. A central aspect of these studies should be the analysis of fret dynamics in response to environmental changes. Evidence exists that frets are not static but flexible (6). Structural flexibility of the fret regions should be seen in context with recent observations that the overall thylakoid architecture is highly dynamic (for example swelling/shrinkage of thylakoid lumen, partial destacking of grana, reviewed in 15, 16). It is likely that swelling/shrinkage of the lumen and/or partial destacking have direct impact on grana-stroma lamellae junctions, i.e. they could control transport processes between stacked and unstacked membrane regions by modifying the fret architecture. Almost no information is available about the factors that control thylakoid membrane dynamics. Some evidence exists that osmotic effects could be involved (17 and references therein). In illuminated samples, photosynthetic electron transport leads to a build-up of a proton motive force (pmf, lumen positive). The pmf can trigger ion fluxes across the thylakoid membrane facilitated by specific ion transporters or channels. In particular, the influx of chloride into the lumen (18, 19) could cause an increase in osmotic potential leading to water influx and swelling of the lumen. Therefore, knowledge about the role of ion transporters and channels in thylakoid membranes and their regulation (18, 19 for recent reviews) is central to understanding architectural thylakoid membrane dynamics. The field of ion movement across photosynthetic

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membranes has become a highly active research field in the last few years and promises interesting discoveries in the near future. Structural dynamics of the stroma gap between adjacent membranes in stacked grana seems less pronounced compared to the lumen (17). However, small changes in the stroma gap could control the distribution between stacked and unstacked regions for protein complexes with significant stromal protrusions as recently postulated for the cyt b6f complex (20). It has to be determined how significant dynamics of the stroma gap are. But some flexibility is expected since the stroma facing membrane side is the place where thylakoid proteins get phosphorylated. It is known that reversible protein phosphorylation at the stroma side changes membrane-membrane interactions that determine the size of the stroma gap (21).

B. Other Photosynthetic Organisms Compared to the thylakoid membrane system of higher plants, the overall architecture of photosynthetic membranes in the model green algae Chlamydomonas reinhardtii is similar but also reveals interesting differences (8). For example, the number of membranes per grana stack in Chlamydomonas is smaller (averaging 3 membranes per stack) and the length of grana is more variable with a tendency of being wider than in higher plants. Also, Chlamydomonas thylakoid membranes possess so-called ‘fenestrations’ (8) as was reported earlier for cyanobacteria (22, 23). Fenestrations are perforations in (stacked) thylakoid membranes filled with stroma and are missing in higher plant thylakoid membranes. Their function is unclear but may allow better diffusion of stroma components (8). A further long-known difference in thylakoid dynamics between higher plants and green algae is the higher magnitude for so called state transitions in algae. In photosynthetic organisms, state transitions regulate a balanced energy distribution between both photosystems by reversible

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redistribution of LHCII (or phycobilisomes in cyanobacteria) from PSII to PSI (16, 24-28). LHCII redistribution is controlled by reversible LHCII phosphorylation catalyzed by STN7 (plants) or STT7 (green algae) kinases. The original hypothesis on state transition is that in state 1, LHCII binds to PSII whereas in state 2 a fraction of LHCII that is phosphorylated decouples from PSII and docks to PSI to serve as a light harvester for this photosystem. Recently, this view was challenged in a way that only a certain fraction of unbound and phosphorylated LHCII binds to PSI and the remaining LHCII fraction is neither bound to both photosystems and is likely in an energy quenched state (29-32). However, irrespective of the fate of phosphorylated and unbound LHCII, the magnitude of LHCII involved in state transitions is significantly higher in green algae compared to higher plants. Recent estimates give about 40% of LHCII involved in state transition in green algae (30 and references therein) whereas this number is only 10-20% in higher plants (24, 26, 34, 35). The reason for this difference is largely obscure. Since the protein building blocks in green algae and higher plants involved in state transition are very similar, a potential explanation could be differences in physicochemical membrane properties in both clades that allow easier lateral redistribution and phosphorylation of LHCII in green algae. Thylakoid membranes are capable of altering their rigidity as demonstrated by state 2 triggered massive increases in membrane undulation in Chlamydomonas (31) or light-induced changes in membrane softness and undulation in cyanobacteria (38). Changes in thylakoid membrane elasticity in general and induced by state transition in particular deserve further studies because they might control essential biomembrane functions like protein mobility. In this respect, an interesting difference between higher plants and green algae (and mosses and ferns) is that the latter contain special betain lipids that are not present in higher plants (39, 40). The most prominent betain lipid is the zwitterionic Diacylglyceryl-N,N,N- trimethylhomoserine (DGTS). A

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scenario is possible that special lipids in green algae lead to an obligatory higher membrane elasticity giving phosphorylated grana proteins more mobility facilitating state transitions. A straightforward possibility to test the role of DGTS for membrane elasticity would be to study structural alterations of thylakoid membranes induced by state transition in DGTS knock-down or knock out mutants. Structural alterations can be measured by cryo-ET (focusing on destacking and membrane undulations) and neutron scattering analysis under state 1 and state 2 conditions. Extending these studies to higher plants under state 1 and state 2 conditions could solve the questions whether membrane elasticity differences exist in both clades. Ultrastructural analysis of the thylakoid membrane system in the model moss Physcomitrella patens reveals a similar overall thylakoid membrane architecture with a similar ratio of stacked to unstacked thylakoid membranes (about 65%) as higher plants (41). Also, the lateral segregation of PSI and PSII to unstacked and stacked thylakoid regions is similar in P. patens as in higher plants (41). This indicates that the overall membrane architecture in mosses and higher plants are similar. However, ultrastructural studies on the thylakoid membrane system of mosses are rare. Since functional processes of energy conversion and their regulation respond very sensitively to slight changes of the thylakoid architecture, more studies are required to understand structural membrane dynamics in mosses. Readers with further interest in thylakoid organization in different groups of oxygenic phototrophs are referred to (42).

The mesoscopic (supramolecular) level – several 100 nm length scale – Mesoscopic physics is a well-defined subdiscipline in condensed matter physics that deals with properties on intermediate length scales ranging from atoms or molecules to micrometer-sized ensembles. In photosynthesis research, the mesoscopic level can be defined in an analog way, i.e.

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it describes the dynamic behavior of protein ensembles on the few 10 nm to micrometer length scales. The mesoscopic scale therefore bridges the structural level between single photosynthetic (super)complexes and the whole thylakoid membrane. The rational to define this structural level is that studying protein ensemble dynamics requires specific techniques and is described by its own set of theories.

A. Higher Plants

In the last decade, studies on the mesoscopic level of photosynthetic membranes have experienced a renaissance mainly because of technical improvements. It becomes clearer that protein ensembles in stacked grana thylakoid membranes of higher plants respond dynamically to changes in environmental conditions (e.g. 16, 43-45). These supramolecular dynamics were either visualized directly by electron or atomic force microscopy (e.g. 46-50) or indirectly by spectroscopic methods (e.g.51). It is important to distinguish between long-term and short-term alterations of the mesoscopic protein arrangement in thylakoid membranes. On the long-term, abiotic factors (in particular light intensity and quality) control the protein composition and organization by retrograde signaling that includes sensing of the status of the photosynthetic apparatus, signal transduction, and processing of signals that eventually leads to differential gene expressions and compositional alterations of the thylakoid membrane (52-54). Short-term supramolecular alterations, in contrast, are triggered by post-translational protein modifications (phosphorylation, protonation, reduction/oxidation) independent on changes of the protein composition. Here, only short-term effects are considered. The interested reader is referred to (3, 55, 56) for long-term changes in thylakoid composition.

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The most obvious short-term supramolecular changes in thylakoid membranes are (i) the reorganization and clustering of part of the light harvesting system of PSII (LHCII) into certain regions of the grana (47, 48) and (ii) a macroscopic switch from a disordered protein arrangement to a highly ordered semicrystalline state (reviewed in 43). There might be more (subtle) mesoscopic alterations in response to environmental factors but they are not well described or are simply not discovered so far. Why is the exact mesoscopic organization of protein complexes in photosynthetic membranes important to understand? Because two fundamental processes of energy conversion are dependent on the supramolecular protein organization: light harvesting and lateral membrane diffusion.

Light harvesting by ultrafast radiationless exciton energy transfer between photosynthetic pigments (chlorophylls and carotenoids) are strongly dependent on the exact positioning (distance and orientation) of the pigments (57). Within single pigment-protein complexes, like photosystems or LHCs, light-harvesting and energy transfer was evolutionary optimized by establishing a specific amino-acid scaffold that tunes the positioning and chemical pigment environment for high-efficient energy transfer. However, the modular organization of the lightharvesting system of PSII (a core dimer surrounded by several layers of monomeric and trimeric LHCIIs with different binding strengths) also requires lateral inter-molecular energy transfer between LHCIIs within the membrane. This implies that the exact mesoscopic arrangement (distance and orientation) of LHCIIs and PSII in grana is crucial for light harvesting. This is readily demonstrated by the observation that a small dilution of the natural high protein packing density in grana causes a significant decrease in light-harvesting efficiency because of a slight separation of LHCII from PSII (58-60). Consequently, the reorganization of LHCIIs and PSIIs in grana membranes reported in the cause of photoprotective energy quenching (abbreviated as qE,

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47, 48) has a huge impact on the energy conversion efficiency of PSII. qE is a central photoprotective mechanism in photosynthetic organisms. In higher plants, it is harbored in the light-harvesting system of PSII and safely converts excess sunlight energy into heat (61-63). It is hypothesized that the mesoscopic rearrangement of LHCIIs and PSIIs under higher light intensities enables qE formation by providing better access of the PsbS protein to energy quenching sites in the dissociated CP24-CP29-LHCII supercomplex (47, 62). However, due to the high sensitivity of intermolecular energy transfer, the mesoscopic reorganization of LHCIIs itself under qE conditions will dramatically effect light harvesting by PSII.

The second process strongly dependent on the supramolecular protein arrangement in thylakoid membranes is lateral diffusion. Grana thylakoid membranes are tightly packed with photosynthetic protein complexes leading to a very high protein area fraction of 0.7 to 0.8 (45, 64), i.e. 70% to 80% of the membrane area is occupied by protein and the rest by lipids. At these high protein concentrations, percolation of small lipophilic tracer molecules (like plastoquinone involved in electron transport or xanthophylls involved in qE) as well as of larger protein complexes (required for PSII repair and state transition) through a membrane crowded with diffusion obstacles is challenging (45, 65). This is a particular problem for lateral diffusion over hundreds of nm from stacked grana to unstacked membrane regions (the grana diameter is about 400 to 500 nm). Monte Carlo-based computer simulations (64-66) and protein diffusion measurements by fluorescence recovery after photobleaching (=FRAP, 50, 67) reveal the severe retardation of long-range diffusion of small (e.g. plastoquinone) or large (e.g. PSII) particles through crowded grana membranes. The FRAP measurements clearly show that macromolecular crowding is responsible for retarded diffusion since dilution of the protein packing density leads to significant faster diffusion (67). Currently, no hypothesis exist how long-range diffusion

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works in crowded grana membranes. It should be kept in mind that high protein densities in grana are required to keep energy transfer between LHCIIs and PSII efficient (see above). Thus, there is a conceptual dilemma that macromolecular crowding is required for efficient light harvesting but causes, on the other hand, severe hindrance of diffusion dependent processes. A first glimpse for a solution for this dilemma comes from computer simulation showing that PQ diffusion in crowded grana is sensitive to the arrangement of the proteins or more precisely to the degree of protein ordering (66). Ordering proteins in grana could be a mechanism to facilitate diffusion in membranes with high obstacle densities (45). The first experimental evidence that supports the facilitating role of protein ordering in grana for lateral diffusion comes from studies on the Arabidopsis fatty acid desaturase 5 mutant (fad5, 50). The fad5 mutant constitutively forms semicrystalline arrays made of PSII supercomplexes and LHCII with high abundance (68). It was shown by FRAP that mobility of small lipophilic molecules is significantly higher in thylakoid membranes of the fad5 mutant compared to wild type plants. Consequently, fad5 plants have faster diffusion-based (plastoquinone) electron transport and diffusion-based conversion of violaxanthin to zeaxanthin required for qE formation (50). Thus, ordering proteins ensures efficient diffusion of small tracers through crowded grana membranes. So why not having constitutive semicrystalline arrays in grana? A possible answer is that semicrystalline proteins come with a cost of a drastically reduced mobility of larger protein complexes. For example, the molecular repair of the vulnerable PSII holocomplex requires migration of damaged PSII from stacked to unstacked regions where the repair machinery is localized (69, 70). It was shown that this long-range diffusion-dependent repair of photodamaged PSII is significantly impaired in fad5 (50) indicating that a disordered state is advantageous for PSII repair. Efficient PSII repair could be, in addition, facilitated by increased mobility of

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photosynthetic complexes that is controlled by STN7/STN8 kinases (71, 72). It follows that mesoscopic switching from disordered to semicryalline protein organizations fine tunes different functions of the photosynthetic apparatus in thylakoid membranes. Depending on environmental conditions, either mobility of small lipophilic molecules is enhanced (semicrystalline state) or of larger protein complexes (disordered state). It must be mentioned that different types of semicrystalline protein arrays in grana exist made of different types of PSII supercomplexes (43) that can have very different impact on lateral membrane mobility (see discussion in 50).

Overall, the mesoscopic protein organization in higher plant thylakoid membranes turns out to be highly dynamic and controlled by environmental cues. A key question is what factors trigger mesoscopic changes and how do these factors connect to the environment of the plant. Two candidates emerged that could control mesoscopic arrangement in grana. The first is the 22 kDa membrane integral PsbS protein.

Evidence exists that PsbS could be involved in

reorganization of grana (47, 62, 73, 74). This protein seems not a part of the PSII-LHCII supercomplex (75) but interacts with free LHCII not strongly bound to PSII (59). Activation of PsbS at low pH values in the thylakoid lumen (pHLumen) by conformational changes induced by protonation of glutamate residues is discussed (76, 77). The pHLumen-triggered structural alterations of the PsbS protein makes a direct bridge to an environmental control on supramolecular reorganizations since pHLumen acts as a sensor for downstream imbalances in energy consumptions. However, the elusive role of PsbS for the supramolecular protein arrangement and a molecular mechanism of how this protein impacts protein organization in grana is far from being solved. Pressing question are: (i) what are the interaction partners of PsbS in grana (first results in 78, 79), (ii) how do interaction partners change from dark to the qE state, (iii) is PsbS directly involved in energy quenching (by providing a quenching site) or indirectly

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by organizing LHCIIs in a quenched supercomplex, (iv) how das PsbS determine protein ordering (e.g. 73), and (v) does PsbS modulate membrane fluidity and protein mobility? Currently, only indirect approaches are available to address these questions. A promising tool for getting mechanistic insights in the interaction between PsbS and LHCIIs and/or PSII complexes is functional studies on compositionally well-defined proteoliposomes (80). The advantage of proteoliposomes is that it allows dissection of the complex protein and protein-lipid interaction networks into simpler subsystem enabling systematic studies of individual interaction but offer the possibility to ramp up complexity by combining components. Furthermore, the lipophilic environment can be easily defined in proteoliposomes, i.e. the differential impact of violaxanthin versus zeaxanthin can be analyzed (80). Complementary to proteoliposomes is cryo SEM on immuno-labeled proteins that could lead to sublocalization of PsbS as well as LHCII- and PSII subunits in the dark and under qE conditions.

A second highly neglected candidate involved in mesoscopic membrane organization is lipids and fatty acids. An intriguing observation is that semicrystalline protein arrays in grana often occur concomitant with phase transition of the main thylakoid lipid monogalatosyldiacylglycerol (MGDG) from a bilayer to a non-bilayer HII phase. This was observed for different non-optimal growth conditions like cold (81), osmotic stress (81), low light (46), as well as in fatty acid mutants (82) that all visualize massive HII formation by EM. However, in addition, HII formation might also occur on a more elusive smaller microscopic scale not detectable by EM (83). These observations indicate that physicochemical properties of the lipid bilayer organize proteins in thylakoid membranes that are further supported by results on the fad5 mutant (see above). Obviously, alteration of thylakoid fatty acids composition (changes in degree of desaturation) links to changes in protein ordering. A critical role of the

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lipid matrix on protein reorganization in grana is further indicated by results on the xanthophyll zeaxanthin (48). Zeaxanthin is formed by the deepoxidation of violaxanthin during the xanthophyll cycle (84). Free zeaxanthin increases the rigidity of thylakoid membranes (85, 86). In this way, accumulation of zeaxanthin in the membrane bilayer could change physicochemical membrane properties in a similar way as fatty acid desaturation. Research on the interrelationship between lipid/fatty acid composition and protein ordering, however, is very rare and deserves much more attention in the future since the composition of lipid bilayers in photosynthetic membranes is under environmental control.

B. Other photosynthetic organisms Protein ordering is more common than generally expected. As in higher plants, photosynthetic membranes in cyanobacteria (87), halobacteria (88), or purple bacteria (89) can arrange into ordered rows or arrays. Similar as for higher plant thylakoid membranes, it is hypothesized for purple bacteria that specific non-random supramamolecular protein organizations are required for efficient lateral quinone diffusion in crowded membranes (90-92). Another aspect that recently gathered more attention is the discovery of spatially confined protein biogenesis and repair zones (42, 93, 94). It seems that bringing proteins together in defined membrane spots in photosynthetic bacteria and green algae is important for the efficiency of protein biogenesis and repair processes. It is hypothesized that these zones ensure that crucial components for protein synthesis and assembly are in physical contact and avoid toxic intermediates by subtract channeling types of reaction mechanisms. Also, futile reaction cycles can be minimized by compartmentalization in these zones since in the course of the multistep protein repair and de novo synthesis forward and backwards reactions have to be organized in a specific sequence, i.e. reassembly after disassembly or dephosphorylation after phosphorylation (in green algae).

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Physical separation of the enzymes catalyzing these reactions in different membrane zones avoids futile reaction cycles. This is a particular problem in bacterial systems that lack macroscopic differentiation in stacked and unstacked thylakoid regions. Evidence exists that grana stacking in higher plants is required to separate distinct enzymes involved in the molecular repair of PSII (95, 96). In difference to higher plants, photosynthetic bacteria seem to solve the challenge of separating biogenesis and repair enzymes by micro-compartmentalization in specialized membrane zones. An interesting problem is how these zones are established, i.e. how to establish high concentration of a certain type of membrane proteins in defined membrane areas. Two proteins are discussed that could be involved in organizing biogenesis centers: CurT in cyanobacteria (97) and VIPP1 in green algae and cyanobacteria (98, 99). However, we are far from having a conclusive model how these proteins organize biogenesis and repair zones.

The molecular level – lipid-protein interactions – Over the past decades, significant progress was made in resolving the molecular architecture of photosynthetic protein complexes, often with atomic resolution. The level of structural details that is available today allows deep understanding of structure-function relationships of individual protein complexes and their evolutionary development (a few non-representative examples are: 100-103). However, an area that is not much researched but is of high physiological relevance is how these complexes interact with their lipidic environment in native photosynthetic membranes or more precisely what is the generic role of physicochemical properties of the lipid bilayer on membrane proteins. What is not meant in this context is the role of lipids that are tightly bound and buried within photosynthetic protein complexes (104). These protein-tethered lipids are resolved in crystallographic data meaning that they have a well-defined binding niche, are

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structurally rigid, and do not exchange with bulk lipids. The interactions of non-protein bound bulk lipids with membrane proteins is a highly active research field in life sciences (see 105 for a recent special issue on this topic) but is still in an early stage for photosynthetic membranes (106). A few studies analyzed the impact of LHCII incorporation into liposomes but the results are conflicting. It was reported that transferring LHCII from a detergent micelle to a lipid bilayer either induces energy quenching (107) or they do not (108). However, as discussed above, good evidence exists that lipids control the mesoscopic protein organization in photosynthetic membranes. Thus, as for other biomembranes, a dynamic interaction between thylakoid membrane lipids and photosynthetic protein complexes exists. What could be the mechanisms how the lipid environment controls protein conformation and organization? A mechanistic bridge between bulk lipids and protein conformation/organization was made by the lateral membrane pressure hypothesis (109) also known as ‘force from lipids’ (FFL) principle (110). Key elements of FFL are specific physicochemical properties of so-called non-bilayer lipids. Non-bilayer lipids are very common in biomembranes. In plants, about 50 mol% of thylakoid lipids is the nonbilayer MGDG. MGDG is thus by far the most abundant lipid in thylakoid membranes and might have special functions in photosynthetic energy conservation (104). In the context of FFL, nonbilayer lipids exert a high physical pressure in the hydrocarbon region of the lipid bilayer because of their bulky fatty acid moiety relative to their small headgroup, i.e. the have an overall conical shape. This lateral pressure induced by non-bilayer lipids forced into the bilayer structure can be sensed by membrane proteins and induces conformational changes, as seen for example for mechanosensitive membrane proteins (111). It is tempting to extrapolate the FFL hypothesis to MGDG containing thylakoid membranes, i.e. that the abundance of non-bilayer MGDG controls the conformation of photosynthetic proteins that in turn determine their supramolecular

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organization. In this context, it is interesting, as mentioned above, that MGDG can phaseseparate into HII phase. The consequence of HII formation is that the abundance of MGDG in the remaining bilayer phase is lower. It follows that the lateral membrane pressure in hydrophobic core of the lipid bilayer decreases. Also, conversion of violaxanthin to zeaxanhin will change the lateral membrane pressure profile. Thus dynamics in the lipid bilayer can have direct consequences on FFL and therefore protein conformation and supramolecular organization. Experimental evidence that supports the role of FFL in thylakoids and on lipid dynamics on protein organization is rare and often indirect. Proteoliposomes of isolated photosynthetic proteins and different but defined mixtures of bilayer and non-bilayer lipids is a promising approach to study FFL for photosynthetic systems.

Outlook Research on photosynthetic energy transformation has been for many decades a highly active research field and attracts scientists from very different disciplines. It is a truly multidisciplinary area. In the last decade, photosynthesis research got an additional momentum in that it offers potential tools for solving pressing problems of mankind in areas of bioenergy, valuable bioproducts, and agriculture. These interactions between basic and applied sciences are fostered by new funding strategies realized in many countries around the globe. Thus, it is expected that photosynthesis research experiences a strong twist towards societal problems. However, these spin-offs of scientific know-how can be only successful with continued and sustained knowledge gained from basic research. In basic photosynthesis research, two tendencies have become apparent in recent years. The first is to study membrane structures and ultrastructures along with their function and

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regulation in their native context (intact cells or leaves). For example, classical room temperature fixation methods of samples for electron microscopy can significantly change structural attributes of the photosynthetic membranes. Therefore, flash freezing techniques like highpressure freezing (samples freeze in 1 ms) becomes important. But also, diverse sets of noninvasive spectroscopic techniques are trimmed and optimized for measurements on highly intact material since isolated systems might lose critical components that characterize the native system. In this respect, in vivo difference and fluorescence spectroscopy is strongly developing and is sometimes connected to high-throughput phenotyping approaches. In addition, neutron scattering is an emerging non-invasive technique that probes periodic membrane attributes. Since neutrons are almost non-invasive to biological membranes and neutron scattering has time resolution that is in the minutes range, this technique allows studying dynamics of thylakoid membranes with intact leaves or cells. The second research trend is to study photosynthetic energy conversion under natural fluctuating environmental conditions. In recent years, it was recognized that many gene products in photosynthetic (and also in non-photosynthetic) organisms deal with adaptation to dynamic environmental features. For unraveling the function of these gene products, measurements must be designed to interrogate the dynamic response of the photosynthetic machinery to natural fluctuations like light intensity.

Acknowledgements

The author acknowledges support from the National Science Foundation (MCB-1616982), the US Department of Energy (DE-SC 0017160), and the USDA National Institute of Food and Agriculture Hatch projects #1005351 and #0119.

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