Abstract

Photosynthetic light reactions proceed in thylakoid membranes (TMs) due to the activity of pigment–protein complexes. These complexes are heterogeneously organized into granal/stromal thylakoids (in plants) or into recently identified cyanobacterial microdomains (MDs). MDs are characterized by specific ratios of photosystem I (PSI), photosystem II (PSII), and phycobilisomes (PBS) and they are visible as sub-micrometer sized areas with different fluorescence ratios. In this report, the process of long-term plasticity in cyanobacterial thylakoid MDs has been explored under variable growth light conditions using Synechocystis sp. PCC6803 expressing YFP tagged PSI. TM organization into MDs has been observed for all categorized shapes of cells independently of their stage in cell cycle. The heterogeneous PSI, PSII, and PBS thylakoid areas were also identified under two types of growth conditions: at continuous light (CL) and at light-dark (L-D) cycle. The acclimation from CL to L-D cycle changed spatial distribution of photosystems, in particular PSI became more evenly distributed in thylakoids under L-D cycle. The process of the spatial PSI (and partially also PSII) redistribution required 1 week and was accompanied by temporal appearance of PBS decoupling probably caused by the re-organization of photosystems. The overall acclimation we observed was defined as TM plasticity as it resembles higher plants grana/stroma reorganization at variable growth light conditions. In addition, we observed large cell to cell variability in the actual MDs organization. It leads us to suggest that the plasticity, and cell to cell variability in MDs could be a manifestation of phenotypic heterogeneity, a recently broadly discussed phenomenon for prokaryotes.

Highlights

  • Photosynthetic light reactions are catalyzed by several protein complexes, namely Photosystem I (PSI), Photosystem II (PSII), cytochrome b6f complex, and ATPase synthase

  • PCC 6803 strains with YFP tagged photosystem I (PSI) (Strašková et al, 2018, 2019) were first cultivated in continuous light (CL) condition and shifted into sinusoidal L-D regime in the bioreactor to study the progressive acclimation of Synechocystis PSI-YFP to the more natural condition mimicing day-night cycle

  • Cell growth was characterized by an increase in optical density measured at 735 nm (OD735) (Figure 1A); it indicted that cells grew only in light period and they stopped growth in the dark

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Summary

Introduction

Photosynthetic light reactions are catalyzed by several protein complexes, namely Photosystem I (PSI), Photosystem II (PSII), cytochrome b6f complex, and ATPase synthase. The light energy needed to drive electron transfer is funneled to the photosystems by light-harvesting antenna complexes in cyanobacteria represented by Phycobilisomes (PBS) They are localized on the TM peripherally attached to the stromal side of PSI and PSII. (Strašková et al, 2019), a heterogeneous distribution of the photosystems has 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. The MD structure is very stable in a span of minutes and it seems to restrict the overall mobility of all PPCs in cyanobacteria thylakoids (Strašková et al, 2019)

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