Complementary Chromatic Adaptation Research Articles

Complementary chromatic adaptation: photoperception to gene regulation

Many photosynthetic organisms can acclimate to the quantity and quality of light present in their environment. In certain cyanobacteria the wavelengths of light in the environment control the synthesis of specific polypeptides of light harvesting antenna complex or phycobilisome. This phenomenon, called complementary chromatic adaptation, is most dramatically observed in comparison of cyanobacteria after growth in green light and red light. In red light-grown cells the phycobilisome is largely composed of phycocyanin and its associated linker polypeptides (the latter are important for the assembly of the phycocyanin subunits and their placement within the light harvesting structure); the organisms appear blue-green color. In green light-grown cells the phycobilisome is largely composed of phycoerythrin and its associated linker polypeptides; the organisms appear red in color. The ways in which these cyanobacteria sense their changing light environment and the regulatory elements involved in controlling the process of complementary chromatic adaptation are discussed in this review.

A phosphorylated DNA‐binding protein is specific for the red‐light signal during complementary chromatic adaptation in cyanobacteria

Complementary chromatic adaptation is a mechanism by which some cyanobacteria that are able to synthesize phycoerythrin can adapt their pigment (phycobiliprotein) content to the incident wavelengths of the light. In Calothrix sp. PCC 7601 it concerns phycoerythrin (cpe operon), synthesized under green light, and phycocyanin-2 (cpc2 operon), expressed under red light, and involves transcriptional controls. With cell-free extracts from Calothrix sp. PCC 7601 grown under various light regimes, a protein designated RcaD was found by gel retardation experiments to specifically bind to the cpc2 promoter region and to be present only in red-light-grown cells. This protein was partially purified and its binding activity was shown to be sensitive to an alkaline phosphatase treatment. RcaD can protect two regions of the cpc2 promoter sequence against degradation by DNase I. Because its activity is detected only under the conditions required for cpc2 expression, we propose that RcaD is a positive effector of transcription.

The phycobilisome, a light-harvesting complex responsive to environmental conditions

Photosynthetic organisms can acclimate to their environment by changing many cellular processes, including the biosynthesis of the photosynthetic apparatus. In this article we discuss the phycobilisome, the light-harvesting apparatus of cyanobacteria and red algae. Unlike most light-harvesting antenna complexes, the phycobilisome is not an integral membrane complex but is attached to the surface of the photosynthetic membranes. It is composed of both the pigmented phycobiliproteins and the nonpigmented linker polypeptides; the former are important for absorbing light energy, while the latter are important for stability and assembly of the complex. The composition of the phycobilisome is very sensitive to a number of different environmental factors. Some of the filamentous cyanobacteria can alter the composition of the phycobilisome in response to the prevalent wavelengths of light in the environment. This process, called complementary chromatic adaptation, allows these organisms to efficiently utilize available light energy to drive photosynthetic electron transport and CO2 fixation. Under conditions of macronutrient limitation, many cyanobacteria degrade their phycobilisomes in a rapid and orderly fashion. Since the phycobilisome is an abundant component of the cell, its degradation may provide a substantial amount of nitrogen to nitrogen-limited cells. Furthermore, degradation of the phycobilisome during nutrient-limited growth may prevent photodamage that would occur if the cells were to absorb light under conditions of metabolic arrest. The interplay of various environmental parameters in determining the number of phycobilisomes and their structural characteristics and the ways in which these parameters control phycobilisome biosynthesis are fertile areas for investigation.

Electron Transport Regulates Cellular Differentiation in the Filamentous Cyanobacterium Calothrix.

Differentiation of the filamentous cyanobacteria Calothrix sp strains PCC 7601 and PCC 7504 is regulated by light spectral quality. Vegetative filaments differentiate motile, gas-vacuolated hormogonia after transfer to fresh medium and incubation under red light. Hormogonia are transient and give rise to vegetative filaments, or to heterocystous filaments if fixed nitrogen is lacking. If incubated under green light after transfer to fresh medium, vegetative filaments do not differentiate hormogonia but may produce heterocysts directly, even in the presence of combined nitrogen. We used inhibitors of thylakoid electron transport (3-[3,4-dichlorophenyl]-1,1-dimethylurea and 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone) to show that the opposing effects of red and green light on cell differentiation arise through differential excitations of photosystems I and II. Red light excitation of photosystem I oxidizes the plastoquinone pool, stimulating differentiation of hormogonia and inhibiting heterocyst differentiation. Conversely, net reduction of plastoquinone by green light excitation of photosystem II inhibits differentiation of hormogonia and stimulates heterocyst differentiation. This photoperception mechanism is distinct from the light regulation of complementary chromatic adaptation of phycobilisome constituents. Although complementary chromatic adaptation operates independently of the photocontrol of cellular differentiation, these two regulatory processes are linked, because the general expression of phycobiliprotein genes is transiently repressed during hormogonium differentiation. In addition, absorbance by phycobilisomes largely determines the light wavelengths that excite photosystem II, and thus the wavelengths that can imbalance electron transport.

Transduction of the light signal during complementary chromatic adaptation in the cyanobacterium Calothrix sp. PCC 7601: DNA-binding proteins and modulation by phosphorylation.

The cyanobacterium Calothrix sp. PCC 7601 can adapt its pigment content in response to changes in the incident light wavelength. It synthesizes, as major light-harvesting pigments, either phycocyanin 2 (PC2, encoded by the cpc2 operon) under red light or phycoerythrin (PE, encoded by the cpeBA operon) under green light conditions. The last step of the signal transduction pathway is characterized by a transcriptional control of the expression of these operons. Partially purified protein extracts were used in gel retardation assays and DNase I footprinting experiments to identify the factors that interact with the promoter region of the cpeBA operon. We found that two proteins, RcaA and RcaB, only detected in extracts of cells grown under green light, behave as positive transcriptional factors for the expression of the cpeBA operon. Treatment of the fractions containing RcaA and RcaB with alkaline phosphatase prevents the binding of RcaA but not of RcaB to the cpeBA promoter region. A post-translational modification of RcaA thus modulates its affinity for DNA.

The phycobilisome, a light-harvesting complex responsive to environmental conditions.

Photosynthetic organisms can acclimate to their environment by changing many cellular processes, including the biosynthesis of the photosynthetic apparatus. In this article we discuss the phycobilisome, the light-harvesting apparatus of cyanobacteria and red algae. Unlike most light-harvesting antenna complexes, the phycobilisome is not an integral membrane complex but is attached to the surface of the photosynthetic membranes. It is composed of both the pigmented phycobiliproteins and the nonpigmented linker polypeptides; the former are important for absorbing light energy, while the latter are important for stability and assembly of the complex. The composition of the phycobilisome is very sensitive to a number of different environmental factors. Some of the filamentous cyanobacteria can alter the composition of the phycobilisome in response to the prevalent wavelengths of light in the environment. This process, called complementary chromatic adaptation, allows these organisms to efficiently utilize available light energy to drive photosynthetic electron transport and CO2 fixation. Under conditions of macronutrient limitation, many cyanobacteria degrade their phycobilisomes in a rapid and orderly fashion. Since the phycobilisome is an abundant component of the cell, its degradation may provide a substantial amount of nitrogen to nitrogen-limited cells. Furthermore, degradation of the phycobilisome during nutrient-limited growth may prevent photodamage that would occur if the cells were to absorb light under conditions of metabolic arrest. The interplay of various environmental parameters in determining the number of phycobilisomes and their structural characteristics and the ways in which these parameters control phycobilisome biosynthesis are fertile areas for investigation.

PHOTOREGULATION OF PHYCOBILISOME STRUCTURE DURING COMPLEMENTARY CHROMATIC ADAPTATION IN THE MARINE CYANOPHYTE PHORMIDIUM SP. C861

ABSTRACTChanges in the molecular structure of phycobilisomes during complementary chromatic adaptation were studied in the marine cyanophyte Phormidium sp. C86. This strain forms phycoerythrin (PE)‐less phycobilisomes under red light but synthesizes PE‐rich phycobilisomes under green light. Analysis of phycobiliprotein composition and electron microscopic examination of phycobilisomes in ultra‐thin sections of cells and of isolated phycobilisomes were performed for cells acclimated to red and green light, respectively. The structure of phycobilisomes formed under red light conditions was typically hemidiscoidal. Phycobilisomes in cells acclimated to green light were twice as large in size as those in cells acclimated to red light. This increase in phycobilisome size was a result of the increase in the molar ratio of antenna pigment (PE and phycocyanin) to allophycocyanin, from 3.5 to 11.3. Pigment composition and fine structure of phycobilisomes formed under green light were similar to those of “nonhemidiscoidal” phycobilisomes reported in Phormidium persicinum. These results suggest that changes occur not only in the molecular species of peripheral rods but also in the structure of rods and probably of cores in relation to their connection with rods during chromatic adaptation of Phormidium sp. C86.

Cyanobacterial Picoplankton from Lake Constance*

AbstractFour types of unicellular cyanobacteria were classified by pigment composition and cell size. These originated from the picoplankton fraction of Lake Constance, Germany. β‐Carotene and zeaxanthin were found to be the main carotenoids of three Synechococcus isolates. In this group, coccoid forms with phycocyanin‐rich phycobilisomes also produce caloxanthin and nostoxanthin, which are xanthophylls with 3 and 4 hydroxy groups, respectively. In addition, these rare carotenoids are observed in rod‐forming Synechococcus isolates which contain phycoerythrin‐rich phycobilisomes, but they are very low or absent in the coccoid phycoerythrin‐rich isolates. Due to size and pigment content the coccoid forms are similar to Synechococcus leopoliensis (SAUG B 1402‐1, formerly Anacystis nidulans) and S. rubescens (SAUG B 3.81) while the rod‐forming isolates differ from S. elongatus (PCC 6716) in phycobilisome composition.The isolate BO 8402 was tentatively assigned to Synechocystis but differs in pigment composition from all strains described as yet. The green cultures exhibited a faint red glow due to an unusual high in vivo autofluorescence from phycocyanin. Neither were phycobilisomes found in a standard preparation nor was allophycocyanin present. The most abundant carotenoids are β‐carotene and caloxanthin, while zeaxanthin, with 12 % of all colored carotenoids, is low.All forms described in this paper lack complementary chromatic adaptation, indicating that the pigment composition is a reliable parameter to identify these freshwater isolates.

Hormogonium Differentiation in the Cyanobacterium Calothrix: A Photoregulated Developmental Process.

Hormogonium differentiation is part of the developmental cycle in many heterocystous cyanobacteria. Hormogonia are involved in the dispersal and survival of the species in its natural habitat. The formation of these differentiated filaments has been shown to depend on several environmental conditions, including spectral light quality. We report here morphological and ultrastructural changes associated with the formation of hormogonia, as well as optimal light conditions required for their differentiation in the cyanobacterium Calothrix sp PCC 7601. The action spectrum for hormogonium differentiation is similar to that which triggers complementary chromatic adaptation because red and green radiation display antagonistic effects in both cases. However, these two photoregulated processes also show major differences. Transcription analyses of genes that are specifically expressed during hormogonium differentiation, as well as of genes encoding phycobiliproteins, suggest that two different photoregulatory pathways may exist in this cyanobacterium.

Pigment chromatic adaptation in Cyclotella caspia Grunow (Bacillariophyta)

The diatom Cyclotella caspia Grunow, isolated from surface waters of the Ubatuba region (Sao Paulo State, Brazil) was submitted to different light spectral distributions for examination of its adaptative response. Growth rate and the photosynthetic pigments chlorophyll a, chlorophyll c, carotenoids and phaeopigments were measured under white, blue and red light of the same intensity (8 and 20 µE.cm-2.s-1). Growth rate increased under blue light while red light increased chl a concentration. The relative proportion of chl a and carotenoids did not change, demonstrating the absence of complementary chromatic adaptation.

Pigment chromatic adaptation in Cyclotella caspia Grunow (Bacillariophyta)

The diatom Cyclotella caspia Grunow, isolated from surface waters of the Ubatuba region (São Paulo State, Brazil) was submitted to different light spectral distributions for examination of its adaptative response. Growth rate and the photosynthetic pigments chlorophyll a, chlorophyll c, carotenoids and phaeopigments were measured under white, blue and red light of the same intensity (8 and 20 µE.cm-2.s-1). Growth rate increased under blue light while red light increased chl a concentration. The relative proportion of chl a and carotenoids did not change, demonstrating the absence of complementary chromatic adaptation.

Chromatic adaptation and the events involved in phycobilisome biosynthesis

Abstract. The major light‐harvesting complex in cyanobacteria and red algae is the phycobilisome, a macromolecular complex that is attached to the surface of the photosynthetic membranes. The phycobilisome is composed of a number of different chromophoric polypeptides called phycobiliproteins and nonchromophoric polypeptides called linker proteins. Several environmental parameters modulate the synthesis, assembly and degradation of phycobilisome components. In many cyanobacteria, the composition of the phycobilisome can change to accommodate the prevalent wavelengths of light in the environment. This phenomenon is called complementary chromatic adaptation. Organisms that exhibit complementary chromatic adaptation must perceive the wavelengths of light in the environment and transduce the light signals into a sequence of biochemical events that result in altering the activities of genes encoding specific phycobiliprotein and linker polypeptides. Other environmental parameters such as light intensity and nutrient status can also have marked effects on both the number and composition of the phycobilisomes. The major concern of this article is the molecular events involved in chromatic adaptation. Most of the information concerning this process has been gained from studies involving the filamentous cyanobacterium Fremyella diplosiphon. However, also briefly considered are some of the complexities involved in phycobilisome biosynthesis and degradation; they include post‐translational modification of phycobilisome polypeptides, the coordinate expression of chromophore and apobiliprotein, the specific degradation of phycobilisomes when cyanobacteria are deprived of macronutrients such as nitrogen, sulphur and phosphorus, and the assembly of the individual phycobilisome components into substructures of the light harvesting complex.

Characterization of the light-regulated operon encoding the phycoerythrin-associated linker proteins from the cyanobacterium Fremyella diplosiphon

Many biological processes in photosynthetic organisms can be regulated by light quantity or light quality or both. A unique example of the effect of specific wavelengths of light on the composition of the photosynthetic apparatus occurs in cyanobacteria that undergo complementary chromatic adaptation. These organisms alter the composition of their light-harvesting organelle, the phycobilisome, and exhibit distinct morphological features as a function of the wavelength of incident light. Fremyella diplosiphon, a filamentous cyanobacterium, responds to green light by activating transcription of the cpeBA operon, which encodes the pigmented light-harvesting component phycoerythrin. We have isolated and determined the complete nucleotide sequence of another operon, cpeCD, that encodes the linker proteins associated with phycoerythrin hexamers in the phycobilisome. The cpeCD operon is activated in green light and expressed as two major transcripts with the same 5' start site but differing 3' ends. Analysis of the kinetics of transcript accumulation in cultures of F. diplosiphon shifted from red light to green light and vice versa shows that the cpeBA and cpeCD operons are regulated coordinately. A common 17-base-pair sequence is found upstream of the transcription start sites of both operons. A comparison of the predicted amino acid sequences of the phycoerythrin-associated linker proteins CpeC and CpeD with sequences of other previously characterized rod linker proteins shows 49 invariant residues, most of which are in the amino-terminal half of the proteins.

Molecular characterization and evolution of sequences encoding light-harvesting components in the chromatically adapting cyanobacterium Fremyella diplosiphon

The major light-harvesting complex in eukaryotic red algae and prokaryotic cyanobacteria is the phycobilisome, a water-soluble complex located on the outer surface of the photosynthetic membranes and composed of both pigmented phycobiliproteins (85%) and non-pigmented linker (15%) polypeptides. The phycobiliproteins are encoded by a gene family and exhibit varying degrees of sequence homology (25 to 55%). Some cyanobacteria can maximize the absorption of prevalent wavelengths of light by adjusting the phycobiliprotein composition of the phycobilisome, a process called complementary chromatic adaptation. In the chromatically adapting species Fremyella diplosiphon, there are at least two sets of phycocyanin genes; one is transcribed as two red light-induced transcripts and the other is encoded on a single transcript present in both red and green light. We have determined the complete nucleotide sequences of both sets of phycocyanin subunit genes and their associated 5′ and 3′ regulatory regions. Based on S 1 nuclease protection experiments, the transcripts (1600 and 3800 bases) encoding the inducible phycocyanin subunits have the same 5′ end, and possible mechanisms for their synthesis are presented. The 5′ end of the 1500-base transcript encoding the constitutive phycocyanin subunits was determined and revealed an Escherichia coli-like “-10” and “-35” region, and sequences near the transcription initiation site homologous to the analogous region of the phycocyanin gene set of Anabaena sp. 7120. Determination of the 3′ ends of the transcripts encoding both F. diplosiphon phycocyanin gene sets revealed regions of potential secondary structure that may be important for transcription termination and/or transcript stability. In addition, the sequence of an open reading frame (encoding a 30 kDa polypeptide), located 3′ to the constitutive phycocyanin gene set in F. diplosiphon and highly conserved in at least three cyanobacterial species, is presented. The same high degree of sequence homology between the two F. diplosiphon PC α and PC β sequences (85 and 77%, respectively) was found at both the nucleotide and amino acid levels, and similar results were obtained for interspecies comparisons. Implications of these homologies with regard to the evolution of phycobiliprotein subunits are discussed.

Characterization of phycobiliprotein and linker polypeptide genes in Fremyella diplosiphon and their regulated expression during complementary chromatic adaptation

Phycobilisomes, comprised of both chromophoric (phycobiliproteins) and non-chromophoric (linker polypeptides) proteins, are light-harvesting complexes present in the prokaryotic cyanobacteria and the eukaryotic red algae. Many cyanobacteria exhibit complementary chromatic adaptation, a process which enables these organisms to optimize absorption of prevalent wavelengths of light by altering the composition of the phycobilisome. To examine the mechanisms involved in adjusting the levels of phycobilisome components during complementary chromatic adaptation, we have isolated and sequenced genes encoding phycobiliprotein and linker polypeptides in the cyanobacterium Fremyella diplosiphon, analyzed their transcriptional characteristics (transcript sizes and abundance when F. diplosiphon is grown in different light qualities) and mapped transcript initiation and termination sites. Our results demonstrate that genes encoding phycobilisome components are often cotranscribed as polycistronic messenger RNAs. Light quality regulates the composition of the phycobilisome by causing changes in the abundance of transcripts encoding specific components, suggesting that regulation is at the level of transcription (although not eliminating the possibility of changes in mRNA stability). The work presented here sets the foundation for analyzing the evolution of the different phycobilisome components and exploring signal transduction from photoperception to activation of specific genes using in vivo and in vitro genetic technology.

Isolation and characterization of light-regulated phycobilisome linker polypeptide genes and their transcription as a polycistronic mRNA.

Several cyanobacteria adjust both the phycobiliprotein and linker protein composition of the phycobilisome, a light-harvesting complex in cyanobacteria and some eucaryotic algae, to maximize absorption of prevalent wavelengths of light. This process is called complementary chromatic adaptation. We sequenced the amino terminus of a linker polypeptide which is associated with phycocyanin and accumulates to high levels during growth of the cyanobacterium Fremyella diplosiphon in red light. A mixed oligonucleotide encoding a region of this amino terminus was synthesized and used to identify a fragment of F. diplosiphon genomic DNA encoding the linker polypeptide. This linker gene was located between two other linker genes and contiguous to the red-light-induced phycocyanin gene set. Sequences of all three linker genes are presented. These genes were transcribed together onto a large polycistronic mRNA which also encoded the red-light-induced phycocyanin subunits. The relationship of this transcript to the biogenesis of the phycobilisome when F. diplosiphon is grown under different conditions of illumination is discussed.

Photosynthetic and pigment responses of sea-ice microalgae to changes in light intensity and quality

Responses of sea-ice microalgae to changes in light intensity and quality were studied from March to May 1983 on the first-year ice of southeastern Hudson Bay (Canadian Arctic). Photosynthetic parameters P B max , α B and β B of the ice algae progressively increased throughout the sampling season. This increase paralleled the under-ice irradiance; it also paralleled the progressive increase of the diatom Nitzschia frigida in the population, from ≈45% of the cells at the end of March to almost 100% in May. The photosynthetic efficiency ( α B ) and several other photosynthetic parameters doubled when the algae were incubated under blue light, as compared with white light. This result stresses the importance of considering the photosynthetically usable radiant energy (PUR) rather than the photosynthetically available radiation (PAR), when measuring photosynthetic responses to light colour. Ice algae generally had high concentrations of chlorophyll c, which could be an adaptive response to their blue-green light environment. When incubated under white illumination, which corresponded to widening the light spectrum, the algae responded by increasing their proportions of carotenoids and chlorophyll c. These changes were in agreement with the theory of complementary chromatic adaptation. The bottom ice environment of Hudson Bay being limited by light intensity and nutrient resources, the ability to chromatically adapt may become a critical factor in species competition.

Green light induces transcription of the phycoerythrin operon in the cyanobacteriumCalothrix7601

Phycobilisomes, the major light-harvesting complexes of cyanobacteria are multimolecular structures made up of chromophoric proteins called phycobiliproteins and non chromophoric linker polypeptides. We report here the isolation and nucleotide sequence of the genes, cpeA and cpeB, which in Calothrix PCC 7601 encode the alpha and beta subunits of phycoerythrin, one of the major phycobiliproteins. In Calothrix PCC 7601, modulation of the polypeptide composition of the phycobilisomes occurs in response to changes of the light wavelength, a phenomenon known as complementary chromatic adaptation. Under green illumination, cells synthesize phycoerythrin and its two specifically associated linker polypeptides (LR35 and LR36), while under red illumination none of these proteins are detected. Using specific probes, a single transcript (1450 nucleotide long) corresponding to the cpe genes was detected but only in green-light-grown cells, establishing the occurrence of transcriptional regulation for the expression of this operon in response to light wavelength changes. The size of this transcript excludes the possibility that the phycoerythrin-associated LR35 and LR36 could be cotranscribed with the cpeA and cpeB genes.

EFFECTS OF PHOTON FLUENCE RATE AND LIGHT SPECTRUM COMPOSITION ON GROWTH, PHOTOSYNTHESIS AND PIGMENT RELATIONS IN GRACILARIA SP.1

ABSTRACTThe optimal photon fluence rate for growth of tha llus tips of Gracilaria sp. was low (about 100 μE·–2·1); higher photon fluence rates inhibited growth. Both phycoerythrin (PE) and chlorophyll (chl) contents decreased with increasing photon fluence rates (up to 100 μE·–m–2s–1) in a fashion inverse to the growth response. Chl/PE ratios varied directly as the growth response over a larger photon fluence rate range. The peak chl/PE ratios were obtained at a photon fluence rate optimal for growth, suggesting that this parameter may be used to estimate in situ growth rates. A low compensation point (about 7 μE·–2s–1) was observed for low light (15 μE·–2s–1) grown plants. This compensation point was also obtained for growth in the long–term (5–6 weeks) experiments. Plants grown at 60 and 140 μE·–2s–1 showed higher light compensation and saturation points, suggesting that the variations in pigment composition found between the different treatments determine the photosynthetic responses at sub–optimal photon fluence rates. Photosynthetic rates at light saturation were the same, on a biomass basis, for plants grown at the various photon fluence rates. Thus, the photosynthetic dark reactions were not influenced by previous light regimes. It is suggested that maximal photosynthetic rates expressed on a biomass basis better reflect the potential productivity at tight saturation than if expressed on a pigment basis. Gracilaria sp. grew better under non–filtered fluorescent and greenish than under reddish and blue–enriched light of equal and sub–optimal photon, fluence rate. However, the pigment relations of the algae did not change in a direction complementary to the light composition at which they grew. This, together with the relatively higher photosynthetic rates under reddish and blueish light for plants previously grown under reddish and blueish light, suggests that adaptations to variouslight spectra are based on mechanisms different from complementary chromatic adaptation of the pigments.

A PHYSIOLOGICAL TEST OF THE THEORY OF COMPLEMENTARY CHROMATIC ADAPTATION. II. BROWN, GREEN AND RED SEAWEEDS1

ABSTRACTThe effect of light quantity (irradiance) on the photosynthetic physiology of seven seaweed species was distinguished from the effect of light quality (color). Plants were grown in outdoor, continuous‐flow tanks, at irradiances saturating and limiting to growth, and in spectral distributions that were either broadband (white) or narrowband (green). The green light field complemented the absorptance spectrum of phycoerythrin and approximated the spectral distribution of a submarine light field in turbid coastal water near the compensation depth. Physiological measurements, made after 6–15 days growth, included light‐harvesting pigment densities, instantaneous photosynthesis‐light relationships and growth rate. In all experiments, these photosynthetic properties were independent of spectral distribution (color) and in most experiments were dependent on irradiance. These data do not conform to the predictions of the theory of complementary chromatic adaptation for seaweeds.