Protein arrangement factor: a new photosynthetic parameter characterizing the organization of thylakoid membrane proteins

Abstract

A proper spatial distribution of photosynthetic pigment‐protein complexes – PPCs (photosystems, light‐harvesting antennas) is crucial for photosynthesis. In plants, photosystems I and II (PSI and PSII) are heterogeneously distributed between granal and stromal thylakoids. Here we have described similar heterogeneity in the PSI, PSII and phycobilisomes (PBSs) distribution in cyanobacteria thylakoids into microdomains by applying a new image processing method suitable for the Synechocystis sp. PCC6803 strain with yellow fluorescent protein‐tagged PSI. The new image processing method is able to analyze the fluorescence ratios of PPCs on a single‐cell level, pixel per pixel. Each cell pixel is plotted in CIE1931 color space by forming a pixel‐color distribution of the cell. The most common position in CIE1931 is then defined as protein arrangement (PA) factor with xy coordinates. The PA‐factor represents the most abundant fluorescence ratio of PSI/PSII/PBS, the ‘mode color’ of studied cell. We proved that a shift of the PA‐factor from the center of the cell‐pixel distribution (the ‘median’ cell color) is an indicator of the presence of special subcellular microdomain(s) with a unique PSI/PSII/PBS fluorescence ratio in comparison to other parts of the cell. Furthermore, during a 6‐h high‐light (HL) treatment, ‘median’ and ‘mode’ color (PA‐factor) of the cell changed similarly on the population level, indicating that such microdomains with unique PSI/PSII/PBS fluorescence were not formed during HL (i.e. fluorescence changed equally in the whole cell). However, the PA‐factor was very sensitive in characterizing the fluorescence ratios of PSI/PSII/PBS in cyanobacterial cells during HL by depicting a 4‐phase acclimation to HL, and their physiological interpretation has been discussed.

Plasticity of Cyanobacterial Thylakoid Microdomains Under Variable Light Conditions

“…We have identified the ability of cyanobacterial TM to acclimate to the switch in light condition by long-term reorganization of photosystems, especially PSI. Except the TM plasticity, we also observed MDs diversity in population of cells in line with previous results (Konert et al, 2019;Strašková et al, 2019). We have raised a hypothesis that the qualitative switch in PSI organization (more homogeneous PSI distribution during L-D than during CL irradiation; Figure 2C and Supplementary Figure 4) is triggered by the addition of a dark period for L-D cycle.…”

“…Synechocystis PSI-YFP cells were collected from bioreactor on regular intervals and the TM structure of Synechocystis PSI-YFP cells was monitored by confocal microscope (Figure 1B). At the start of the experiment (when cells were still acclimated to CL), thylakoids had characteristic structure, color organization, and intensity as usual photosynthetic MDs in the culture grown under CL conditions (Konert et al, 2019;Strašková et al, 2019), the most typical set-up for laboratory experiments with cyanobacteria. MDs, as they were defined (Strašková et al, 2019), are characterized by typical PSI/PSII/PBS ratios that are reflected in their colors (in RGB color coding) and visible in single-cell images of TMs.…”

“…Recently (Strašková et al, 2019), a heterogeneous distribution of the photosystems has also been identified in cyanobacteria in vivo without changes in membrane stacking. These heterogeneous TM areas were described as MDs (Konert et al, 2019;Strašková et al, 2019) and defined as membrane regions with different composition of pigment-proteins complexes (PPCs), it means photosystems and PBS. These special membrane zones, sub-micrometer in size, define the mosaic-like structure of TM.…”

Photosynthesis—European Congress on Photosynthesis Research

“…A number of articles treat regulatory aspects of photosystem II (Shevela et al ), the plastoquinone pool (Borisova‐Mubarakshina et al ), cytochrome c (Bernal‐Bayard et al ), redox regulation (Nikkanen et al ), photoacclimation (Hu et al ) and photorespiration (García‐Caledrón et al ). The growing interest in structural aspects is shown by articles on the dynamics of the thylakoid membrane (Solovchenko et al , Konert et al , Ughy et al ) and of specific proteins (Carius et al , Vojta and Fulgosi ), protein complexes (Kuthanová Trsková et al , Fedorov et al ) and the antenna (Albanese et al , Kuthanová Trsková et al 2019). An important tool for photosynthesis research is variable chlorophyll fluorescence, which is used to study photosystem II in isolated form, in thylakoid membranes as well as in vivo.…”

“…and theoretical and experimental consideration on the water-splitting complex (Capone et al 2019, Yamaguchi et al 2019, Chatterjee et al 2019) and photosystem I (Santabarbara et al 2019a) to more integrated aspects of photosynthesis research (Buezo et al 2019, Hamdani et al 2019, Ptushenko and Ptushenko 2019, Hernández-Prieto et al 2019, Krieger-Liszkay et al 2019). A number of articles treat regulatory aspects of photosystem II (Shevela et al 2019), the plastoquinone pool (Borisova-Mubarakshina et al 2019), cytochrome c (Bernal-Bayard et al 2019), redox regulation (Nikkanen et al 2019), photoacclimation (Hu et al 2019) and photorespiration (García-Caledrón et al 2019).The growing interest in structural aspects is shown by articles on the dynamics of the thylakoid membrane(Solovchenko et al 2019, Konert et al 2019, Ughy et al 2019 and of specific proteins (Carius et al 2019, Vojta and Fulgosi 2019), protein complexes (Kuthanová Trsková et al 2019, Fedorov et al 2019) and the antenna (Albanese et al 2019, Kuthanová…”