The use of far-red light (FRL) is observed in some cyanobacteria, as well as in some marine and freshwater algae. While algae mobilize FRL absorbing antenna, which contains common chlorophyll a (Chl a), cyanobacteria produce red-shifted Chl d and/or Chl f. These pigments are synthesized either irrespective of ambient light or synthesized during FRL photoacclimation (FaRLiP), or adaptive remodeling of photosynthetic apparatus induced by relative enrichment with FRL quanta. The presence of red-shifted chlorophylls as well as their functions and topography are registered with various methods based on fluorescence measurement, such as: (1) steady-state fluorescence detection in live cells, cell fractions, and photosynthetic apparatus constituents; (2) time-resolved fluorescence spectroscopy, which traces energy transfer between individual pigments; (3) confocal laser scanning microscopy (CLSM), which helps to localize photosynthetic pigments in situ. This chapter describes photosynthetic apparatus in cyanobacteria and their photoacclimation phenomena. Over past decades, FRL photoacclimation has been studied in a small number of cyanobacteria. Novel Chl f-producing strains Chlorogloeopsis sp. CALU 759 and Synechocystis sp. CALU 1173 would represent promising model objects. Importantly, although they belong to alternative morphotypes and distant phylogenetic lineages, fluorescence pattern of their FRL-grown cells similarly falls within general FaRLiP response.
- chlorophylls d and f
- steady-state fluorescence detection
- time-resolved fluorescence spectroscopy
- confocal laser scanning microscopy
Cyanobacteria are the only up-to-date known prokaryotes capable of oxygenic photosynthesis. They assimilate light energy via electron transfer from water to oxidized ferredoxin, and excrete triplet dioxygen as a waste product. The majority of cyanobacteria possess chlorophyll
This chapter includes four sections, which describe: photosynthetic apparatus in cyanobacteria; photoacclimation phenomena in cyanobacteria; fluorescence methods employed in the study of FRL-adapting cyanobacteria; FRL photoacclimating strains in CALU collection (St. Petersburg University, St. Petersburg, Russia).
2. Photosynthetic apparatus in cyanobacteria
Light energy assimilation machinery in cyanobacteria is usually localized in/on intracytoplasmic membrane structures termed thylakoids. Among principal constituents are: reaction centers (RC) of two photosystems (PSs), a main light-harvesting complex (LHC), and electron transfer chain (ETC). The essential component of PSII is unique light-dependent enzyme—H2O dehydrogenase, or water oxidizing complex (WOC).
In the majority of cyanobacteria, Chl
Both PSs are supplied with their respective light-harvesting antennae, which contain Chl
3. Photoacclimation phenomena in cyanobacteria
Cyanobacteria can acclimate themselves to light quantity and quality, that is, they adaptively respond to the shifts in ambient light color and intensity. For this purpose, they can modulate: (1) PS content, (2) the interaction between PS and PBS, and (3) LHC structure, PBP content in particular.
In the first case, antenna size varies inversely with a flood of light quanta. This strategy is performed via the changes in thylakoid surface and PS packing density .
In the second case (given that ambient light is enriched with either short- or long-wavelength quanta), excitation energy equally distributes between long-wavelength PSI and short-wavelength PSII. This phenomenon is termed State 1 ↔ State 2 transition. State 1 is achieved in response to relative over-excitation of PSII . Here, PBS behaves as a mobile antenna, and it laterally moves from PSII to PSI. In the opposite situation (State 2), PBS detaches from PSI and comes back to PSII . State transition scenario is as follows: up- or downshifts in ETC reduction level → redox-sensitive (de)phosphorylation of proteins within the PBS baseplate → coulomb attraction/repulsion between PBS and PS .
In the third case, PBS absorbance peak adjusts to ambient light color (preferentially green or red). This adaptation is performed via the shifts in PE (green light absorbing PBP) and PC (red light absorbing PBP) content. The knowledge on this phenomenon termed complementary chromatic adaptation (CA) has been comprehensively reviewed [16, 17].
In agreement with a response to green or red light, cyanobacteria have been ascribed to three CA groups : group СА1 (steady PE and PC content), group СА2 (PE content varies), and group СА3 (PE and PC contents vary).
Groups CA2 and CA3 are specified according to the presence of regulatory photoreceptors CcaS and RcaE, which belong to the “cyanobacteriochromes” phytochrome family [19, 20, 21]. These receptors contain one and the same bilin-binding domain GAF (cyclic guanosine monophosphate phosphodiesterase/adenylyl cyclase/FhlA), which regulates green or red light-triggered photocycle [22, 23]. In the case of CA2, under green light, CcaS (signal transducer) phosphorylates transcription factor CcaR (response regulator) that induces the production of PE . In the case of CA3, under red light, RcaE phosphorylates transcription factors RcaF and RcaC, which regulate numerous participants of PC and PE biosynthesis pathway [23, 24].
Group CA4 is represented by marine
Group CA5 is typical of
Group CA6 is represented by several strains of cyanobacteria, which adaptively produce Chl
Group CA7  has been described in the case of cyanobacteria which synthesize yellow-green light absorbing PEC, and regulate the amount of this PBP light dependently. Similar to СА2, the adaptive response is under control of two-component regulatory system CcaS/CcaR.
Another type of reaction to green or red light is typical for СА0 group . In this case, PBP content is stable, while the amount of CpcG2 (CpcL) and CpcG1 linker polypeptides varies reciprocally . In green light, the CcaS/CcaR system upgrades the production of CрcG2 (CpcL) linker involved in the biogenesis of APC lacking PBS . The CрcG2 (CpcL) type PBS is suggested to be rod-like, and it possibly supplies energy to PSI under suboptimal conditions [16, 22].
Cyanobacterial response to FRL has been described in cyanobacteria only recently, and it is based on red-shifted Chl
Cyanobacteria can use two main strategies of FRL photoacclimation.
In the first strategy, Chl
In the second strategy, Chl
FaRLiP response falls under the control of two-component phosphorelay system . Sensory component (RfpA photoreceptor) represents a far-red light regulated cyanobacteriochrome with histidine kinase domain. Response regulators RfpB and RfpC have two CheY-like signal accepting domains, which flank the DNA-binding domain. RfpB acts as a transcription activator for FaRLiP genes [47, 50]. Within this phoshorelay, RfpA histidine kinase becomes (de)activated, and that influences the RfpB key response regulator. In its turn, RfpC is involved in transfer of phosphoryl group from RfpA to RfpB.
4. Fluorescence methods employed in the research of far-red light-adapting cyanobacteria
4.1 Steady-state fluorescence detection
Absorbed energy of light quanta brings photosynthetic pigments into excited state, which is relaxed by: (1) productive energy assimilation in the form of charge separation within RC, (2) counterproductive energy dissipation into heat, or with fluorescence quanta . Since the photosynthetic apparatus is less than 100% effective, the second mechanism is universally in action, although it depends on environmental and physiological regimes.
Steady-state fluorescence detection helps to identify photosynthetic pigments because they demonstrate individual fluorescence excitation and emission spectra. Additionally, this method can detect energy transfer between pigments. Fluorescence spectra can be obtained at either room or cryogenic temperature (most frequently, 77 K). Low temperatures are preferred because of lowered molecular mobility, and due to smaller intramolecular vibrations; as a result, peaks become higher and better resolved . Importantly, low-temperature regime (4–77 K) helps to discriminate PSI chlorophyll (~ 720 nm) and PSII chlorophyll (~ 685 nm) emission peaks [51, 52, 53].
Current data on steady-state fluorescence of red-shifted chlorophylls are few. For instance, the spectra of WL-grown
Apart from the experiments on cell suspensions, steady-state fluorescence of Chl
Cryogenic detection helped to monitor energy transfer in FRL-adapted
Steady-state fluorescence emission was also detected in the experiments with PBP-specific 590-nm excitation of RL- or FRL-grown
4.2 Time-resolved fluorescence spectroscopy
The method helps to analyze molecular processes within a picosecond/nanosecond timescale . Because primary photosynthetic processes take several femtoseconds/nanoseconds, time-resolved fluorescence spectroscopy can trace corresponding rates and pathways of energy transfer . Recently, this method has helped to elucidate the role(s) of red-shifted chlorophylls in cyanobacterial PS.
In the case of Chl
Time-resolved fluorescence detection within a picosecond/femtosecond time-scale was also performed with
Later, the reality of uphill energy transfer from Chl
At the same time, the involvement of red-shifted chlorophylls in charge separation within PSI and PSII was proposed for
Room temperature and 77 K fluorescence data in unicellular strain KC1 producing Chl
Similarly, femtosecond pump-probe spectroscopy of
Time-resolved fluorescence spectroscopy also helped to analyze energy transfer in RL-or FRL-grown cells of
4.3 Confocal laser scanning microscopy (CLSM)
The method is based on the auto fluorescence of photosynthetic pigments, chlorophylls in the first instance . CLSM permits to distinguish individual pigments based on their emission peaks, to evaluate peak intensity, and to localize pigments in situ. Highly sensitive up-to-date CLSM microscopes help to obtain 3D images of cells and tissues, and to analyze dynamic physiological processes. Unfortunately, the potentiality of this method, at least with regard to FRL-adapting cyanobacteria, is underestimated, and thus corresponding data are few.
CLSM has been applied to the study of Chl
Anisotropic distribution of pigments was also observed in
5. Far-red light photoacclimating strains in the CALU collection
5.1 Growth conditions
An ability of FRL-dependent synthesis of Chl
Liquid cultures were grown for a 2- to 3-week time in modified BG-11 medium , at 20–22°С, under permanent WL (500 lx) or FRL illumination (LED with ~750 nm emission maximum).
5.2 Steady-state fluorescence detection protocol
Cell pellet was washed with 100 mM HEPES buffer (pH 8.0), and resuspended in 50 mM HEPES (pH 8.0) with or without the addition of 25% glycerol. Room temperature fluorescence was detected in a Cary Eclipse scanning spectrophotometer/fluorimeter (Agilent Technologies, Santa Clara, CA, USA), and obtained data were treated with a Cary Eclipse Scan program. Emission spectra were detected for excitation at 440 nm (specific for chlorophyll) and 550 nm (specific for PBP). Excitation spectra (chlorophyll fluorescence at 745 nm) were also detected.
5.3 CLSM protocol
The method helped to reveal photosynthetic pigments topography. Life preparations of WL- or FRL-grown cells were observed in a Leica TCS SP5 MP STED confocal microscope (Leica Microsystems GmbH, Germany). Fluorescence was raised with a 458-nm-wavelength nitrogen laser. The images were obtained in XYZ scanning regime with a 0.5-μm step. The following emission channels were used: 560–600 nm (PE), 620–650 nm (PC), 670–700 nm (Chl
5.4 Steady-state fluorescence detection of chlorophylls and phycobiliproteins in white light- or far-red light-grown cells
Fluorescence emission spectra (Figures 2(a,b) and 3(a,b)) obtained at chlorophyll-specific 440-nm excitation demonstrated 670–740 nm maxima. In WL-grown
Fluorescence emission spectra obtained with PBP-specific 590-nm excitation resulted in 645–660 nm emission peak with broad 690–715 nm shoulder. In WL-grown
In FR-grown cells, larger size 645–660 nm peak was attended with smaller 715–725 nm peak (Figures 2(d) and 3(d)). Modified emission spectra, as compared with WL-grown cells, could be explained by some changes in PBS arrangement and behavior during the FaRLiP response [45, 48, 49].
The comparison of emission spectra in Figures 2 and 3 showed that, in the case of FRL-grown cells, direct excitation of chlorophylls (blue light excitation, 440-nm wavelength) was more efficient than via antenna PBP pigments (550-nm green light exciting mainly PE and PC). This effect can be explained by PBS uncoupling with PSII because bulk fluorescence at room temperature is known to issue from PSII. If not coupled, PBP excited at 550 nm should exhibit considerable fluorescence around 700 nm (that is the case here).
Fluorescence excitation spectra of WL-grown cells (Figures 2(e) and 3(e)) demonstrated a single peak at 625–650 nm excitation wavelength. Negligible fluorescence during illumination with 400–500 nm light (which preferentially excited chlorophylls) can be explained by shading of the blue region with photosynthetically inactive carotenoids. At the same time, fluorescence during illumination with ~600 nm (which preferentially excited PBP) raised a maximum chlorophyll fluorescence that additionally indicated an efficient coupling of PBS with PSII. In contrast to WL-grown cells, in FRL-grown cells (Figures 2(f) and 3(f)), peak chlorophyll fluorescence was observed at ~670 and ~ 720 nm excitation. High ratio of 720-nm peak/670-nm peak size additionally witnesses for a change of photosynthetic apparatus at FaRLiP response. It is noteworthy that unlike cryogenic method, room temperature fluorescence detection could not comment on the specificity of Chl
5.5 CLSM of chlorophylls and phycobiliproteins in white light- and far-red light-grown cells
In the case of WL-grown
Similar topology was observed in FRL-grown
In the case of FRL-grown
Over past decades, FaRLiP photoacclimation has been studied in many respects, although in a small number of cyanobacterial strains . In this connection, novel Chl
The authors are grateful to St. Petersburg University Research Center “Cultivation of microorganisms” (http://researchpark.spbu.ru/collection-ccem-rus/1628-ccem-kollekciya-calu-rus) for a help with strains maintenance. They also thank St. Petersburg University Research Centers “Molecular and Cell Technologies” and “Chromas” for research fellowship. The work was supported by the Russian Foundation for Fundamental Research, project no. 20-04-00020.
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