Nejvíce citovaný článek - PubMed ID 22402228
The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition
Cyanobacteria hold great potential to revolutionize conventional industries and farming practices with their light-driven chemical production. To fully exploit their photosynthetic capacity and enhance product yield, it is crucial to investigate their intricate interplay with the environment including the light intensity and spectrum. Mathematical models provide valuable insights for optimizing strategies in this pursuit. In this study, we present an ordinary differential equation-based model for the cyanobacterium Synechocystis sp. PCC 6803 to assess its performance under various light sources, including monochromatic light. Our model can reproduce a variety of physiologically measured quantities, e.g. experimentally reported partitioning of electrons through four main pathways, O2 evolution, and the rate of carbon fixation for ambient and saturated CO2. By capturing the interactions between different components of a photosynthetic system, our model helps in understanding the underlying mechanisms driving system behavior. Our model qualitatively reproduces fluorescence emitted under various light regimes, replicating Pulse-amplitude modulation (PAM) fluorometry experiments with saturating pulses. Using our model, we test four hypothesized mechanisms of cyanobacterial state transitions for ensemble of parameter sets and found no physiological benefit of a model assuming phycobilisome detachment. Moreover, we evaluate metabolic control for biotechnological production under diverse light colors and irradiances. We suggest gene targets for overexpression under different illuminations to increase the yield. By offering a comprehensive computational model of cyanobacterial photosynthesis, our work enhances the basic understanding of light-dependent cyanobacterial behavior and sets the first wavelength-dependent framework to systematically test their producing capacity for biocatalysis.
- MeSH
- biologické modely * MeSH
- fotosyntéza * fyziologie MeSH
- fykobilizomy metabolismus MeSH
- koloběh uhlíku fyziologie MeSH
- oxid uhličitý metabolismus MeSH
- počítačová simulace MeSH
- světlo * MeSH
- Synechocystis * metabolismus fyziologie MeSH
- výpočetní biologie MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- fykobilizomy MeSH
- oxid uhličitý MeSH
The investigation of spatial heterogeneity within the thylakoid membrane (TM) proteins has gained increasing attention in photosynthetic research. The recent advances in live-cell imaging have allowed the identification of heterogeneous organisation of photosystems in small cyanobacterial cells. These sub-micrometre TM regions, termed microdomains in cyanobacteria, exhibit functional similarities with granal (Photosystem II dominant) and stromal (Photosystem I dominant) regions observed in TM of higher plants. This study delves into microdomain heterogeneity using super-resolution Airyscan-based microscopy enhancing resolution to approximately ~125 nm in x-y dimension. The new data reveal membrane areas rich in Photosystem I within the inner TM rings. Moreover, we identified analogous dynamics in the mobility of Photosystem II and phycobilisomes; countering earlier models that postulated differing mobility of these complexes. These novel findings thus hold significance for our understanding of photosynthesis regulation, particularly during state transitions.
- Klíčová slova
- Airyscan, FRAP, cyanobacteria, microdomain, photosystem, protein mobility, super-resolution microscopy, thylakoid membrane heterogeneity,
- Publikační typ
- časopisecké články MeSH
Oxygenic photosynthesis takes place in thylakoid membranes (TM) of cyanobacteria, algae, and higher plants. It begins with light absorption by pigments in large (modular) assemblies of pigment-binding proteins, which then transfer excitation energy to the photosynthetic reaction centers of photosystem (PS) I and PSII. In green algae and plants, these light-harvesting protein complexes contain chlorophylls (Chls) and carotenoids (Cars). However, cyanobacteria, red algae, and glaucophytes contain, in addition, phycobiliproteins in phycobilisomes that are attached to the stromal surface of TM, and transfer excitation energy to the reaction centers via the Chl a molecules in the inner antennas of PSI and PSII. The color and the intensity of the light to which these photosynthetic organisms are exposed in their environment have a great influence on the composition and the structure of the light-harvesting complexes (the antenna) as well as the rest of the photosynthetic apparatus, thus affecting the photosynthetic process and even the entire organism. We present here a perspective on 'Light Quality and Oxygenic Photosynthesis', in memory of George Christos Papageorgiou (9 May 1933-21 November 2020; see notes a and b). Our review includes (1) the influence of the solar spectrum on the antenna composition, and the special significance of Chl a; (2) the effects of light quality on photosynthesis, measured using Chl a fluorescence; and (3) the importance of light quality, intensity, and its duration for the optimal growth of photosynthetic organisms.
Light plays an essential role in photosynthesis; however, its excess can cause damage to cellular components. Photosynthetic organisms thus developed a set of photoprotective mechanisms (e.g., non-photochemical quenching, photoinhibition) that can be studied by a classic biochemical and biophysical methods in cell suspension. Here, we combined these bulk methods with single-cell identification of microdomains in thylakoid membrane during high-light (HL) stress. We used Synechocystis sp. PCC 6803 cells with YFP tagged photosystem I. The single-cell data pointed to a three-phase response of cells to acute HL stress. We defined: (1) fast response phase (0-30 min), (2) intermediate phase (30-120 min), and (3) slow acclimation phase (120-360 min). During the first phase, cyanobacterial cells activated photoprotective mechanisms such as photoinhibition and non-photochemical quenching. Later on (during the second phase), we temporarily observed functional decoupling of phycobilisomes and sustained monomerization of photosystem II dimer. Simultaneously, cells also initiated accumulation of carotenoids, especially ɣ-carotene, the main precursor of all carotenoids. In the last phase, in addition to ɣ-carotene, we also observed accumulation of myxoxanthophyll and more even spatial distribution of photosystems and phycobilisomes between microdomains. We suggest that the overall carotenoid increase during HL stress could be involved either in the direct photoprotection (e.g., in ROS scavenging) and/or could play an additional role in maintaining optimal distribution of photosystems in thylakoid membrane to attain efficient photoprotection.
- Klíčová slova
- Synechocystis, carotenoids, high light, microdomains, non-photochemical quenching, photoinhibition, photoprotection, photosystems, thylakoid membrane,
- MeSH
- bakteriální proteiny genetika metabolismus MeSH
- fotosystém I - proteinový komplex genetika metabolismus MeSH
- fotosystém II - proteinový komplex genetika metabolismus MeSH
- karotenoidy metabolismus MeSH
- světlo * MeSH
- Synechocystis metabolismus účinky záření MeSH
- tylakoidy metabolismus účinky záření MeSH
- velikost buňky účinky záření MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- bakteriální proteiny MeSH
- fotosystém I - proteinový komplex MeSH
- fotosystém II - proteinový komplex MeSH
- karotenoidy MeSH
Five macrolichens of different thallus morphology from Antarctica (King George Island) were used for this ecophysiological study. The effect of thallus desiccation on primary photosynthetic processes was examined. We investigated the lichens' responses to the relative water content (RWC) in their thalli during the transition from a wet (RWC of 100%) to a dry state (RWC of 0%). The slow Kautsky kinetics of chlorophyll fluorescence (ChlF) that was recorded during controlled dehydration (RWC decreased from 100 to 0%) and supplemented with a quenching analysis revealed a polyphasic species-specific response of variable fluorescence. The changes in ChlF at a steady state (Fs), potential and effective quantum yields of photosystem II (FV/FM, ΦPSII), and nonphotochemical quenching (NPQ) reflected a desiccation-induced inhibition of the photosynthetic processes. The dehydration-dependent fall in FV/FM and ΦPSII was species-specific, starting at an RWC range of 22-32%. The critical RWC for ΦPSII was below 5%. The changes indicated the involvement of protective mechanisms in the chloroplastic apparatus of lichen photobionts at RWCs of below 20%. In both the wet and dry states, the spectral reflectance curves (SRC) (wavelength 400-800 nm) and indices (NDVI, PRI) of the studied lichen species were measured. Black Himantormia lugubris showed no difference in the SRCs between wet and dry state. Other lichens showed a higher reflectance in the dry state compared to the wet state. The lichen morphology and anatomy data, together with the ChlF and spectral reflectance data, are discussed in relation to its potential for ecophysiological studies in Antarctic lichens.
- Klíčová slova
- King George Island, chlorophyll fluorescence, lichen dehydration, maritime antarctica, stress tolerance,
- Publikační typ
- časopisecké články MeSH
Photomorphogenesis is a process by which photosynthetic organisms perceive external light parameters, including light quality (color), and adjust cellular metabolism, growth rates and other parameters, in order to survive in a changing light environment. In this study we comprehensively explored the light color acclimation of Cyanobium gracile, a common cyanobacterium in turbid freshwater shallow lakes, using nine different monochromatic growth lights covering the whole visible spectrum from 435 to 687 nm. According to incident light wavelength, C. gracile cells performed great plasticity in terms of pigment composition, antenna size, and photosystem stoichiometry, to optimize their photosynthetic performance and to redox poise their intersystem electron transport chain. In spite of such compensatory strategies, C. gracile, like other cyanobacteria, uses blue and near far-red light less efficiently than orange or red light, which involves moderate growth rates, reduced cell volumes and lower electron transport rates. Unfavorable light conditions, where neither chlorophyll nor phycobilisomes absorb light sufficiently, are compensated by an enhanced antenna size. Increasing the wavelength of the growth light is accompanied by increasing photosystem II to photosystem I ratios, which involve better light utilization in the red spectral region. This is surprisingly accompanied by a partial excitonic antenna decoupling, which was the highest in the cells grown under 687 nm light. So far, a similar phenomenon is known to be induced only by strong light; here we demonstrate that under certain physiological conditions such decoupling is also possible to be induced by weak light. This suggests that suboptimal photosynthetic performance of the near far-red light grown C. gracile cells is due to a solid redox- and/or signal-imbalance, which leads to the activation of this short-term light acclimation process. Using a variety of photo-biophysical methods, we also demonstrate that under blue wavelengths, excessive light is quenched through orange carotenoid protein mediated non-photochemical quenching, whereas under orange/red wavelengths state transitions are involved in photoprotection.
- Klíčová slova
- cyanobacteria, imbalance, light-quality acclimation, photosynthesis, pigment composition,
- Publikační typ
- časopisecké články MeSH
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.
- Klíčová slova
- cyanobacteria, membrane organization, microdomains and rafts, phenotypic heterogeneity, photosynthesis, photosystems, phycobilisomes decoupling, thylakoid membrane,
- Publikační typ
- časopisecké články MeSH
Cold acclimation modifies the photosynthetic machinery and enables plants to survive at sub-zero temperatures, whereas in warm habitats, many species suffer even at non-freezing temperatures. We have measured chlorophyll a fluorescence (ChlF) and CO2 assimilation to investigate the effects of cold acclimation, and of low temperatures, on a cold-sensitive Arabidopsis thaliana accession C24. Upon excitation with low intensity (40 µmol photons m- 2 s- 1) ~ 620 nm light, slow (minute range) ChlF transients, at ~ 22 °C, showed two waves in the SMT phase (S, semi steady-state; M, maximum; T, terminal steady-state), whereas CO2 assimilation showed a linear increase with time. Low-temperature treatment (down to - 1.5 °C) strongly modulated the SMT phase and stimulated a peak in the CO2 assimilation induction curve. We show that the SMT phase, at ~ 22 °C, was abolished when measured under high actinic irradiance, or when 3-(3, 4-dichlorophenyl)-1, 1- dimethylurea (DCMU, an inhibitor of electron flow) or methyl viologen (MV, a Photosystem I (PSI) electron acceptor) was added to the system. Our data suggest that stimulation of the SMT wave, at low temperatures, has multiple reasons, which may include changes in both photochemical and biochemical reactions leading to modulations in non-photochemical quenching (NPQ) of the excited state of Chl, "state transitions," as well as changes in the rate of cyclic electron flow through PSI. Further, we suggest that cold acclimation, in accession C24, promotes "state transition" and protects photosystems by preventing high excitation pressure during low-temperature exposure.
- Klíčová slova
- 3-(3, 4-dichlorophenyl)-1, 1- dimethylurea, Chlorophyll fluorescence transients, Cold acclimation, Gas-exchange measurements, Low-temperature effect, Methyl viologen, Slow SMT fluorescence phase, State transition,
- MeSH
- aklimatizace MeSH
- Arabidopsis metabolismus MeSH
- chlorofyl a metabolismus MeSH
- fotosyntéza fyziologie MeSH
- nízká teplota MeSH
- teplota MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- chlorofyl a MeSH
The slow kinetic phases of the chlorophyll a fluorescence transient (induction) are valuable tools in studying dynamic regulation of light harvesting, light energy distribution between photosystems, and heat dissipation in photosynthetic organisms. However, the origin of these phases are not yet fully understood. This is especially true in the case of prokaryotic oxygenic photoautotrophs, the cyanobacteria. To understand the origin of the slowest (tens of minutes) kinetic phase, the M-T fluorescence decline, in the context of light acclimation of these globally important microorganisms, we have compared spectrally resolved fluorescence induction data from the wild type Synechocystis sp. PCC 6803 cells, using orange (λ = 593 nm) actinic light, with those of mutants, ΔapcD and ΔOCP, that are unable to perform either state transition or fluorescence quenching by orange carotenoid protein (OCP), respectively. Our results suggest a multiple origin of the M-T decline and reveal a complex interplay of various known regulatory processes in maintaining the redox homeostasis of a cyanobacterial cell. In addition, they lead us to suggest that a new type of regulatory process, operating on the timescale of minutes to hours, is involved in dissipating excess light energy in cyanobacteria.
- Klíčová slova
- Fluorescence quenching, Interplay of regulatory processes, Kautsky effect, Photoprotection, Synechocystis, The M–T phase,
- MeSH
- bakteriální proteiny genetika metabolismus MeSH
- chlorofyl a MeSH
- chlorofyl chemie genetika metabolismus MeSH
- diuron chemie MeSH
- fluorescence MeSH
- fluorescenční spektrometrie MeSH
- fykobilizomy genetika metabolismus MeSH
- kyanid draselný chemie MeSH
- luminiscenční měření MeSH
- světlo MeSH
- Synechocystis chemie genetika metabolismus MeSH
- teplota MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- bakteriální proteiny MeSH
- chlorofyl a MeSH
- chlorofyl MeSH
- diuron MeSH
- fykobilizomy MeSH
- kyanid draselný MeSH
- orange carotenoid protein, Synechocystis MeSH Prohlížeč
