Distribution of excitation energy in photosynthesis: quantification of fluorescence yields from intact cyanobacteria

doi:10.1016/0022-2313(92)90021-Z

Journal of Luminescence

Volume 51, Issues 1–3, February 1992, Pages 91-98

https://doi.org/10.1016/0022-2313(92)90021-Z Get rights and content

Abstract

Fluorescence emission spectra of intact cyanobacteria in state 1 and state 2 were determined at 77 K. Spectra were obtained from samples held in a rotating cuvette designed to average sample inhomogeneities and allow accurate fluorescence yield comparisons without normalization to intrinsic or added fluorophore emission peaks. Emission spectra obtained for excitation in the chlorophyll a (Chl a) and phycobilisome absorption regions were modelled with a sum of components representing phycobilin and Chl a fluorescence emission bands. Our results show that the transition from state 1 to state 2 is characterized by a large decrease in the amplitude of the fluorescence emission from the photosystem 2 associated Chl a components, and a small increase in the amplitude of the emission from the photosystem 1 associated Chl a component for excitation of either Chl a or the PBS. The results are discussed with respect to three models for regulation of the distribution of excitation energy (light state transition) between photosystem 2 and photosystem 1 in cyanobacteria.

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Cited by (32)

State transitions in cyanobacteria studied with picosecond fluorescence at room temperature
2020, Biochimica et Biophysica Acta - Bioenergetics
Citation Excerpt :
A decrease of the absorption cross-section/functional antenna size of PSII in state II was ascribed earlier to migration of PBSs from PSII to PSI in the mobile antenna model [15–18]. The spillover model [20,50–52] on the other hand, ascribed quenching of PSII in state II to EET to PSI, whereas also a combination of both models was proposed [20,25]. All these models predict an increase of EET to PSI in state II at the expense of excitations in PSII.
Cyanobacteria can rapidly regulate the relative activity of their photosynthetic complexes photosystem I and II (PSI and PSII) in response to changes in the illumination conditions. This process is known as state transitions. If PSI is preferentially excited, they go to state I whereas state II is induced either after preferential excitation of PSII or after dark adaptation. Different underlying mechanisms have been proposed in literature, in particular i) reversible shuttling of the external antenna complexes, the phycobilisomes, between PSI and PSII, ii) reversible spillover of excitation energy from PSII to PSI, iii) a combination of both and, iv) increased excited-state quenching of the PSII core in state II. Here we investigated wild-type and mutant strains of Synechococcus sp. PCC 7942 and Synechocystis sp. PCC 6803 using time-resolved fluorescence spectroscopy at room temperature. Our observations support model iv, meaning that increased excited-state quenching of the PSII core occurs in state II thereby balancing the photochemistry of photosystems I and II.
State transitions in the cyanobacterium Synechococcus elongatus 7942 involve reversible quenching of the photosystem II core
2018, Biochimica et Biophysica Acta - Bioenergetics
Citation Excerpt :
In [8,28,29] 77 K steady-state spectra of Synechocystis PCC 6803 and Synechococcus 7002 (normalized either to PSI emission, PBS emission, or an internal fluorescent probe) showed that the ratio of PBS/PSI emission remained the same in state I and II, which is in agreement with our results (see Fig. 1). However, in [5,30] the 77 K spectra of Synechococcus PCC 7002 and Synechococcus PCC 6301 cells showed an increase of PSI emission in state II upon PBS or Chl a excitation. This is in disagreement with the results of [8,28,29] and our results that showed the PBS/PSI emission ratio does not differ in state I and II.
Cyanobacteria use chlorophyll and phycobiliproteins to harvest light. The resulting excitation energy is delivered to reaction centers (RCs), where photochemistry starts. The relative amounts of excitation energy arriving at the RCs of photosystem I (PSI) and II (PSII) depend on the spectral composition of the light. To balance the excitations in both photosystems, cyanobacteria perform state transitions to equilibrate the excitation energy. They go to state I if PSI is preferentially excited, for example after illumination with blue light (light I), and to state II after illumination with green-orange light (light II) or after dark adaptation. In this study, we performed 77-K time-resolved fluorescence spectroscopy on wild-type Synechococcus elongatus 7942 cells to measure how state transitions affect excitation energy transfer to PSI and PSII in different light conditions and to test the various models that have been proposed in literature. The time-resolved spectra show that the PSII core is quenched in state II and that this is not due to a change in excitation energy transfer from PSII to PSI (spill-over), either direct or indirect via phycobilisomes.
Diverse mechanisms for photoprotection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change
2015, Biochimica et Biophysica Acta - Bioenergetics
Citation Excerpt :
In support of the role of PBS mobility in state transitions, the presence of high concentrations of phosphate, sucrose, glutaraldehyde, or betaine has been shown to lock-in the preexisting light state and inhibit PBS movement [229,231–233,243]. Mobile PBS finely explains the redistribution of phycobilin absorbed excitation energy during state transitions, yet it is unable to explain the changes in Chl absorbed excitation energy, thereby the necessity for inclusion of the spillover mechanism [235,244–247]. Both mobile PBS and spillover mechanisms are now believed to contribute to state transitions [160,161,187,229,235,248], with a greater magnitude of energy redistribution likely from mobile PBS under natural light conditions, since spillover might only occur during dark adaption [229].
Photosystem II (PSII) of photosynthesis catalyzes one of the most challenging reactions in nature, the light driven oxidation of water and release of molecular oxygen. PSII couples the sequential four step oxidation of water and two step reduction of plastoquinone to single photon photochemistry with charge accumulation centers on both its electron donor and acceptor sides. Photon capture, excitation energy transfer, and trapping occur on a much faster time scale than the subsequent electron transfer and charge accumulation steps. A balance between excitation of PSII and the use of the absorbed energy to drive electron transport is essential. If the absorption of light energy increases and/or the sink capacity for photosynthetically derived electrons decreases, potentially deleterious side reactions may occur, including the production of reactive oxygen species. In response, a myriad of fast (second to minutes timescale) and reversible photoprotective mechanisms are observed to regulate PSII excitation when the environment changes more quickly than can be acclimated to by gene expression. This review compares the diverse photoprotective mechanisms that are used to dissipate (quench) PSII excitation within the antenna systems of higher land plants, green algae, diatoms, and cyanobacteria. The molecular bases of how PSII excitation pressure is sensed by the antenna system and how the antenna then reconfigures itself from a light harvesting to an energy dissipative mode are discussed.
Astaxanthin production by a highly photosensitive Haematococcus mutant
2012, Process Biochemistry
Citation Excerpt :
After heterotrophically precultured Haematococcus cells were cultivated under autotrophic conditions for 4 days, the vegetative cells were dark-adapted at 23 °C (optimal growth temperature) for 30 min and used for the next step. Chlorophyll fluorescence in Haematococcus cells was measured at 77 K using a FluoroMax-2 spectrofluorimeter (ISA Jobin Yvon-Spex, Edison, NJ, USA) as previously described [13]. All values were corrected by subtracting the background signal from a blank medium and were normalized to a 685 nm centered PSII peak.
Haematococcus pluvialis synthesizes a high yield of astaxanthin using CO₂ in a photoautotrophic culture without contaminant heterotrophs; however, it takes too long to induce astaxanthin production. In this study, a highly photosensitive mutant strain was attained by conventional random mutagenesis and an efficient isolation method to shorten induction time. Sensitivity to photoinhibition in this mutant was raised by a partial lesion in the photosystem II (PSII) of photosynthesis, thereby prompting a change in cellular morphology as well as stimulating carotenogenesis (astaxanthin production). As a result, the concentrations of cell biomass and astaxanthin were dramatically increased by 27% and 62% under strong light and 79% and 153% under moderate light, respectively. This Haematococcus mutant would be useful for the economical astaxanthin production capable of reducing the light energy cost in a photoautotrophic culture system, even in areas with insufficient sunlight.
Changes in cyclic and respiratory electron transport by the movement of phycobilisomes in the cyanobacterium Synechocystis sp. strain PCC 6803
2007, Biochimica et Biophysica Acta - Bioenergetics
Citation Excerpt :
The major models are the “mobile PBS” model, which involves physical movement of PBS to explain the energy transfer from PBS to PSI [33–35], and the “spillover” model to interpret energy exchange from PSII to PSI, assuming a closer approximation of the two photosystems [36–38]. Others are similar to the two basic models [39–41]. A previous study showed that “mobile PBS” and “spillover” exist simultaneously during light-induced state transitions in cyanobacteria [41].
Phycobilisomes (PBS) are the major accessory light-harvesting complexes in cyanobacteria and their mobility affects the light energy distribution between the two photosystems. We investigated the effect of PBS mobility on state transitions, photosynthetic and respiratory electron transport, and various fluorescence parameters in Synechocystis sp. strain PCC 6803, using glycinebetaine to immobilize and couple PBS to photosystem II (PSII) or photosystem I (PSI) by applying under far-red or green light, respectively. The immobilization of PBS at PSII inhibited the increase in cyclic electron flow, photochemical and non-photochemical quenching, and decrease in respiration that occurred during the movement of PBS from PSII to PSI. In contrast, the immobilization of PBS at PSI inhibited the increase in respiration and photochemical quenching and decrease in cyclic electron flow and non-photochemical quenching that occurred when PBS moved from PSI to PSII. Linear electron transport did not change during PBS movement but increased or decreased significantly during longer illumination with far-red or green light, respectively. This implies that PBS movement is completed in a short time but it takes longer for the overall photosynthetic reactions to be tuned to a new state.
Light-induced excitation energy redistribution in Spirulina platensis cells: "spillover" or "mobile PBSs"?
2004, Biochimica et Biophysica Acta - Bioenergetics
Citation Excerpt :
The “mobile phycobilisome (PBS)” model was proposed by suggesting a physical movement of PBSs, quite analogous to that of Chl a/b-containing organisms [14–16]. Besides, there are also some other models proposed to explain the experimental observations [8,17] but similar to the two basic models mentioned above. In fact, investigation on the state transition is not only for learning the energy regulation mechanism but also for probing the structural matches and functional associations of the three functional groups, PBS, PSII and PSI.
State transitions induced by light and redox were investigated by observing the 77 K fluorescence spectra for the intact cells of Spirulina platensis. To clarify if phycobilisomes (PBSs) take part in the state transition, the contributions of PBSs to light-induced state transition were studied in untreated cells and the cells treated by betaine which fixed PBSs firmly on the thylakoid membranes. It was observed that the betaine-treated cells did not show any light-induced state transition. This result definitely confirmed that the light-induced excitation energy regulation between the two photosystems is mainly dependent on a spatial movement of PBSs on the thylakoid membranes, which makes PBS cores partially decoupled from photosystem II (PSII) while PBS rods more strongly coupled with photosystem I (PSI) during the transition from state 1 to state 2. On the other hand, an energy exchange between the two photosystems was observed in both untreated and betaine-treated cells during redox-induced state transition. These observations suggested that two different mechanisms were involved in the light-induced state transition and the redox-induced one. The former involves only a physical movement of PBSs, while the latter involves not only the movement of PBS but also energy spillover from PSII to PSI. A model for light-induced state transition was proposed based on the current results as well as well known knowledge.

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Distribution of excitation energy in photosynthesis: quantification of fluorescence yields from intact cyanobacteria

Abstract

Biophys. J.

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Biochim. Biophys. Acta

FEBS Lett.

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Biochim. Biophys. Acta