Revisiting cyanobacterial state transitions

Calzadilla, Pablo Ignacio; Kirilovsky, Diana

doi:10.1039/c9pp00451c

Cited by 77 publications

(67 citation statements)

References 159 publications

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“…The periods with excessive light are potentially harmful to photosynthetic proteins, pigments, and lipids due to the formation of ROS (Li et al, 2009). Therefore, there are several photoprotective and lightoptimizing processes (see, e.g., reviews for cyanobacteria; Kirilovsky et al, 2014;Calzadilla and Kirilovsky, 2020) that either dissipate excessive irradiation (non-photochemical quenching), regulate excitation energy distribution into/between photosystems (e.g., state transitions; McConnell et al, 2002;Kaňa et al, 2012;antenna decoupling;Kaňa et al, 2009;Tamary et al, 2012) or they cope with accelerated degradation of proteins in light (e.g., photoinhibition; Li et al, 2018). However, a functional link between the response of TM organization and fluctuations in light is still rather fragmented.…”

Section: Introductionmentioning

confidence: 99%

Plasticity of Cyanobacterial Thylakoid Microdomains Under Variable Light Conditions

2020

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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.

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Section: Introductionmentioning

confidence: 99%

Plasticity of Cyanobacterial Thylakoid Microdomains Under Variable Light Conditions

2020

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“…Similarly, one could expect a similar effect of antenna protein mobilization during state transitions. The process regulates optimal redistribution of excitation energy flow from antennas either to PSI or to PSII [68,69]. In higher plants thylakoids, the redistribution could be allowed by a highly mobile fraction of LHCII antennae, which has been found by FCS in the stromal lamella of Chlamydomonas reinhardtii thylakoids (D LHCII = 0.92-2.13 µm 2 s −1 [47]).…”

Section: Discussionmentioning

confidence: 99%

“…In fact, it has originally been proposed that PBS mobility is the main mechanism of state transitions in cyanobacteria [72]. However, the concept needs to be revised experimentally by further experiments (see discussion in [69]) due to the presence of PBS blinking [73] that has been shown to affect FRAP measurements of mobility in many fluorescent proteins [74,75] including GFP [76].…”

Section: Discussionmentioning

confidence: 99%

Fast Diffusion of the Unassembled PetC1-GFP Protein in the Cyanobacterial Thylakoid Membrane

Kaňa

Steinbach

Sobotka

et al. 2020

Life

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Biological membranes were originally described as a fluid mosaic with uniform distribution of proteins and lipids. Later, heterogeneous membrane areas were found in many membrane systems including cyanobacterial thylakoids. In fact, cyanobacterial pigment–protein complexes (photosystems, phycobilisomes) form a heterogeneous mosaic of thylakoid membrane microdomains (MDs) restricting protein mobility. The trafficking of membrane proteins is one of the key factors for long-term survival under stress conditions, for instance during exposure to photoinhibitory light conditions. However, the mobility of unbound ‘free’ proteins in thylakoid membrane is poorly characterized. In this work, we assessed the maximal diffusional ability of a small, unbound thylakoid membrane protein by semi-single molecule FCS (fluorescence correlation spectroscopy) method in the cyanobacterium Synechocystis sp. PCC6803. We utilized a GFP-tagged variant of the cytochrome b6f subunit PetC1 (PetC1-GFP), which was not assembled in the b6f complex due to the presence of the tag. Subsequent FCS measurements have identified a very fast diffusion of the PetC1-GFP protein in the thylakoid membrane (D = 0.14 − 2.95 µm2s−1). This means that the mobility of PetC1-GFP was comparable with that of free lipids and was 50–500 times higher in comparison to the mobility of proteins (e.g., IsiA, LHCII—light-harvesting complexes of PSII) naturally associated with larger thylakoid membrane complexes like photosystems. Our results thus demonstrate the ability of free thylakoid-membrane proteins to move very fast, revealing the crucial role of protein–protein interactions in the mobility restrictions for large thylakoid protein complexes.

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“…This debate arises from the conspicuous feature of the PBS to bind both PSII and PSI under different light regimes. There are two major hypotheses: the PBS mobile model and the PBS detachment model [58]. In the first model, the PBS remains bound to PSII under red light (State I), since red light preferentially excites PSII rather than PSI and triggers the downstream process of charge separation in the reaction centre [59].…”

Section: Pbs Functioning Under Different Light Conditionsmentioning

confidence: 99%

Light Harvesting in Fluctuating Environments: Evolution and Function of Antenna Proteins across Photosynthetic Lineage

Bag

2021

Plants

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Photosynthesis is the major natural process that can harvest and harness solar energy into chemical energy. Photosynthesis is performed by a vast number of organisms from single cellular bacteria to higher plants and to make the process efficient, all photosynthetic organisms possess a special type of pigment protein complex(es) that is (are) capable of trapping light energy, known as photosynthetic light-harvesting antennae. From an evolutionary point of view, simpler (unicellular) organisms typically have a simple antenna, whereas higher plants possess complex antenna systems. The higher complexity of the antenna systems provides efficient fine tuning of photosynthesis. This relationship between the complexity of the antenna and the increasing complexity of the organism is mainly related to the remarkable acclimation capability of complex organisms under fluctuating environmental conditions. These antenna complexes not only harvest light, but also provide photoprotection under fluctuating light conditions. In this review, the evolution, structure, and function of different antenna complexes, from single cellular organisms to higher plants, are discussed in the context of the ability to acclimate and adapt to cope under fluctuating environmental conditions.

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Revisiting cyanobacterial state transitions

Abstract: Critical evaluation of “new” and “old” models of cyanobacterial state transitions. Phycobilisome and membrane contributions to this mechanism are addressed. The signaling transduction pathway is discussed.

Cited by 77 publications

References 159 publications

Plasticity of Cyanobacterial Thylakoid Microdomains Under Variable Light Conditions

Plasticity of Cyanobacterial Thylakoid Microdomains Under Variable Light Conditions

Fast Diffusion of the Unassembled PetC1-GFP Protein in the Cyanobacterial Thylakoid Membrane

Light Harvesting in Fluctuating Environments: Evolution and Function of Antenna Proteins across Photosynthetic Lineage

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