Investigating the Balance between Structural Conservation and Functional Flexibility in Photosystem I.

Photosynthesis, as the primary source of energy for all life forms, plays a crucial role in maintaining the global balance of energy, entropy, and enthalpy in living organisms. Among its various building blocks, photosystem I (PSI) is responsible for light-driven electron transfer, crucial for generating cellular reducing power. PSI acts as a light-driven plastocyanin-ferredoxin oxidoreductase and is situated in the thylakoid membranes of cyanobacteria and the chloroplasts of eukaryotic photosynthetic organisms. Comprehending the structure and function of the photosynthetic machinery is essential for understanding its mode of action. New insights are offered into the structure and function of PSI and its associated light-harvesting proteins, with a specific focus on the remarkable structural conservation of the core complex and high plasticity of the peripheral light-harvesting complexes.

Leaf photosynthetic and anatomical insights into mechanisms of acclimation in rice in response to long-term fluctuating light.

Long-term fluctuating light (FL) conditions are very common in natural environments. The physiological and biochemical mechanisms for acclimation to FL differ between species. However, most of the current conclusions regarding acclimation to FL were made based on studies in algae or Arabidopsis thaliana. It is still unclear how rice (Oryza sativa L.) integrate multiple physiological changes to acclimate to long-term FL. In this study, we found that rice growth was repressed under long-term FL. By systematically measuring phenotypes and physiological parameters, we revealed that: (a) under short-term FL, photosystem I (PSI) was inhibited, while after 1-7 days of long-term FL, both PSI and PSII were inhibited. Higher acceptor-side limitation in electron transport and higher overall nonphotochemical quenching (NPQ) explained the lower efficiencies of PSI and PSII, respectively. (b) An increase in pH differences across the thylakoid membrane and a decrease in thylakoid proton conductivity revealed a reduction of ATP synthase activity. (c) Using electron microscopy, we showed a decrease in membrane stacking and stomatal opening after 7 days of FL treatment. Taken together, our results show that electron flow, ATP synthase activity and NPQ regulation are the major processes determining the growth performance of rice under long-term FL conditions.

On the origin of oxygenic photosynthesis and Cyanobacteria.

Oxygenic phototrophs have played a fundamental role in Earth's history by enabling the rise of atmospheric oxygen (O2 ) and paving the way for animal evolution. Understanding the origins of oxygenic photosynthesis and Cyanobacteria is key when piecing together the events around Earth's oxygenation. It is likely that photosynthesis evolved within bacterial lineages that are not extant, so it can be challenging when studying the early history of photosynthesis. Recent genomic and molecular evolution studies have transformed our understanding about the evolution of photosynthetic reaction centres and the evolution of Cyanobacteria. The evidence reviewed here highlights some of the most recent advances on the origin of photosynthesis both at the genomic and gene family levels.

Photoprotection of photosystems in fluctuating light intensities.

Oxygenic photosynthetic organisms experience strong fluctuations in light intensity in their natural terrestrial and aquatic growth environments. Recent studies with both plants and cyanobacteria have revealed that Photosystem (PS) I is the potential target of damage upon abrupt changes in light intensity. Photosynthetic organisms have, however, developed powerful mechanisms in order to protect their photosynthetic apparatus against such potentially hazardous light conditions. Although the electron transfer chain has remained relatively unchanged in both plant chloroplasts and their cyanobacterial ancestors, the photoprotective and regulatory mechanisms of photosynthetic light reactions have experienced conspicuous evolutionary changes. In cyanobacteria, the specific flavodiiron proteins (Flv1 and Flv3) are responsible for safeguarding PSI under rapidly fluctuating light intensities, whilst the thylakoid located terminal oxidases are involved in the protection of PSII during 12h diurnal cycles involving abrupt, square-wave, changes from dark to high light. Higher plants such as Arabidopsis thaliana have evolved different protective mechanisms. In particular, the PGR5 protein controls electron flow during sudden changes in light intensity by allowing the regulation mostly via the Cytochrome b6f complex. Besides the function of PGR5, plants have also acquired other dynamic regulatory mechanisms, among them the STN7-related LHCII protein phosphorylation that is similarly responsible for protection against rapid changes in the light environment. The green alga Chlamydomonas reinhardtii, as an evolutionary intermediate between cyanobacteria and higher plants, probably possesses both protective mechanisms. In this review, evolutionarily different photoprotective mechanisms under fluctuating light conditions are described and their contributions to cyanobacterial and plant photosynthesis are discussed.

Energy transfer from phycobilisomes to photosystem I at room temperature.

The phycobilisomes function as the primary light-harvesting antennae in cyanobacteria and red algae, effectively harvesting and transferring excitation energy to both photosystems. Here we investigate the direct energy transfer route from the phycobilisomes to photosystem I at room temperature in a mutant of the cyanobacterium Synechocystis sp. PCC 6803 that lacks photosystem II. The excitation dynamics are studied by picosecond time-resolved fluorescence measurements in combination with global and target analysis. Global analysis revealed several fast equilibration time scales and a decay of the equilibrated system with a time constant of ≈220 ps. From simultaneous target analysis of measurements with two different excitations of 400 nm (chlorophyll a) and 580 nm (phycobilisomes) a transfer rate of 42 ns-1 from the terminal emitter of the phycobilisome to photosystem I was estimated.

Small angle neutron scattering and lipidomic analysis of a native, trimeric PSI-SMALP from a thermophilic cyanobacteria.

The use of styrene-maleic acid copolymers (SMAs) to produce membrane protein-containing nanodiscs without the initial detergent isolation has gained significant interest over the last decade. We have previously shown that a Photosystem I SMALP from the thermophilic cyanobacterium, Thermosynechococcus elongatus (PSI-SMALP), has much more rapid energy transfer and charge separation in vitro than detergent isolated PSI complexes. In this study, we have utilized small-angle neutron scattering (SANS) to better understand the geometry of these SMALPs. These techniques allow us to investigate the size and shape of these particles in their fully solvated state. Further, the particle's proteolipid core and detergent shell or copolymer belt can be interrogated separately using contrast variation, a capability unique to SANS. Here we report the dimensions of the Thermosynechococcus elongatus PSI-SMALP containing a PSI trimer. At ~1.5 MDa, PSI-SMALP is the largest SMALP to be isolated; our lipidomic analysis indicates it contains ~1300 lipids/per trimeric particle, >40-fold more than the PSI-DDM particle and > 100 fold more than identified in the 1JB0 crystal structure. Interestingly, the lipid composition to the PSI trimer in the PSI-SMALP differs significantly from bulk thylakoid composition, being enriched ~50 % in the anionic sulfolipid, SQDG. Finally, utilizing the contrast match point for the SMA 1440 copolymer, we also can observe the ~1 nm SMA copolymer belt surrounding this SMALP for the first time, consistent with most models of SMA organization.

Photosynthetic Parameters Show Specific Responses to Essential Mineral Deficiencies.

In response to decreases in the assimilation efficiency of CO2, plants oxidize the reaction center chlorophyll (P700) of photosystem I (PSI) to suppress reactive oxygen species (ROS) production. In hydro-cultured sunflower leaves experiencing essential mineral deficiencies, we analyzed the following parameters that characterize PSI and PSII: (1) the reduction-oxidation states of P700 [Y(I), Y(NA), and Y(ND)]; (2) the relative electron flux in PSII [Y(II)]; (3) the reduction state of the primary electron acceptor in PSII, QA (1 - qL); and (4) the non-photochemical quenching of chlorophyll fluorescence (NPQ). Deficiency treatments for the minerals N, P, Mn, Mg, S, and Zn decreased Y(II) with an increase in the oxidized P700 [Y(ND)], while deficiencies for the minerals K, Fe, Ca, B, and Mo decreased Y(II) without an increase in Y(ND). During the induction of photosynthesis, the above parameters showed specific responses to each mineral. That is, we could diagnose the mineral deficiency and identify which mineral affected the photosynthesis parameters.

Molecular Mechanism of Oxidation of P700 and Suppression of ROS Production in Photosystem I in Response to Electron-Sink Limitations in C3 Plants.

Photosynthesis fixes CO2 and converts it to sugar, using chemical-energy compounds of both NADPH and ATP, which are produced in the photosynthetic electron transport system. The photosynthetic electron transport system absorbs photon energy to drive electron flow from Photosystem II (PSII) to Photosystem I (PSI). That is, both PSII and PSI are full of electrons. O2 is easily reduced to a superoxide radical (O2-) at the reducing side, i.e., the acceptor side, of PSI, which is the main production site of reactive oxygen species (ROS) in photosynthetic organisms. ROS-dependent inactivation of PSI in vivo has been reported, where the electrons are accumulated at the acceptor side of PSI by artificial treatments: exposure to low temperature and repetitive short-pulse (rSP) illumination treatment, and the accumulated electrons flow to O2, producing ROS. Recently, my group found that the redox state of the reaction center of chlorophyll P700 in PSI regulates the production of ROS: P700 oxidation suppresses the production of O2- and prevents PSI inactivation. This is why P700 in PSI is oxidized upon the exposure of photosynthesis organisms to higher light intensity and/or low CO2 conditions, where photosynthesis efficiency decreases. In this study, I introduce a new molecular mechanism for the oxidation of P700 in PSI and suppression of ROS production from the robust relationship between the light and dark reactions of photosynthesis. The accumulated protons in the lumenal space of the thylakoid membrane and the accumulated electrons in the plastoquinone (PQ) pool drive the rate-determining step of the P700 photo-oxidation reduction cycle in PSI from the photo-excited P700 oxidation to the reduction of the oxidized P700, thereby enhancing P700 oxidation.

Crystal Structure of Photosystem I Monomer From Synechocystis PCC 6803.

A single histidine addition to the C-terminus of PsaL of Synechocystis sp. PCC 6803 was previously reported by our lab to shift the trimer-to-monomer ratio of PSI in favor of the monomeric form. P700 re-reduction and NADP+ photo-reduction measurements of the PsaLHIS strain show no effect on PSI activity in comparison to the WT trimeric PSI. Crystal structure of the PsaLHIS monomeric PSI reveals several alterations that occurred in the trimerisation site of PSI, primarily a deformation of the C-terminus of PsaL and loss of chlorophyll a and ß-carotene molecules.