Photoregulation of cellular morphology during complementary chromatic adaptation requires sensor-kinase-class protein RcaE in Fremyella diplosiphon

We used wild-type UTEX481; SF33, a shortened-filament mutant strain that shows normal complementary chromatic adaptation pigmentation responses; and FdBk14, an RcaE-deficient strain that lacks light-dependent pigmentation responses, to investigate the molecular basis of the photoregulation of cellular morphology in the cyanobacterium Fremyella diplosiphon. Detailed microscopic and biochemical analyses indicate that RcaE is required for the photoregulation of cell and filament morphologies of F. diplosiphon in response to red and green light.     

Convergence and divergence of the photoregulation of pigmentation and cellular morphology in Fremyella diplosiphon

Photosynthetic pigment accumulation and cellular and filament morphology are regulated reversibly by green light (GL) and red light (RL) in the cyanobacterium Fremyella diplosiphon during complementary chromatic adaptation (CCA). The photoreceptor RcaE (regulator of chromatic adaptation), which appears to function as a light-responsive sensor kinase, controls both of these responses. Recent findings indicate that downstream of RcaE, the signaling pathways leading to light-dependent changes in morphology or pigment synthesis and/or accumulation branch, and utilize distinct molecular components. We recently reported that the regulation of the accumulation of the GL-absorbing photosynthetic accessory protein phycoerythrin (PE) and photoregulation of cellular morphology are largely independent, as many mutants with severe PE accumulation defects do not have major disruptions in the regulation of cellular morphology. Furthermore, morphology can be disrupted under GL without impacting GL-dependent PE accumulation. Most recently, however, we determined that the disruption of the cpeR gene, which encodes a protein that is known to function as an activator of PE synthesis under GL, results in disruption of cellular morphology under GL and RL. Thus, apart from RcaE, CpeR is only the second known regulator to impact morphology under both light conditions in F. diplosiphon.     

Energy transfer processes in Gloeobacter violaceus PCC 7421 that possesses phycobilisomes with a unique morphology

We examined energy transfer dynamics in phycobilisomes (PBSs) of cyanobacteria in relation to the morphology and pigment compositions of PBSs. We used Gloeobacter violaceus PCC 7421 and measured time-resolved fluorescence spectra in three types of samples, i.e., intact cells, PBSs, and rod assemblies separated from cores. Fremyella diplosiphon, a cyanobacterial species well known for its complementary chromatic adaptation, was used for comparison after growing under red or green light. Spectral data were analyzed by the fluorescence decay-associated spectra with components common in lifetimes with a time resolution of 3 ps/channel and a spectral resolution of 2 nm/channel. This ensured a higher resolution of the energy transfer kinetics than those obtained by global analysis with fewer sampling intervals. We resolved four spectral components in phycoerythrin (PE), three in phycocyanin (PC), two in allophycocyanin, and two in photosystem II. The bundle-like PBSs of G. violaceus showed multiple energy transfer pathways; fast ( approximately 10 ps) and slow ( approximately 100 ps and approximately 500 ps) pathways were found in rods consisting of PE and PC. Energy transfer time from PE to PC was two times slower in G. violaceus than in F. diplosiphon grown under green light.     

Effects of glucose during photoheterotrophic growth of the cyanobacterium <Emphasis Type="Italic">Calothrix</Emphasis> sp. PCC 7601 capable for chromatic adaptation

Photoheterotrophic growth of a filamentous cyanobacterium Calothrix sp. PCC 7601, which is capable for complementary chromatic adaptation, in the presence of glucose was accompanied by changes in the content of phycobiliproteins. Glucose, a source of energy and a metabolism regulator, differently affected the level of major phycobilisome pigments, phycocyanin (PC) and phycoerythrin (PE) in the cells. When red light enhanced PC synthesis, glucose enhanced it additionally. When green light suppressed PC synthesis, glucose did not affect it. Under both light regimes, glucose inhibited PE synthesis. Thus, glucose oppositely affected the content of two major phycobiliproteins. Glucose not only affected the ratio between phycobiliproteins but also decreased the content of carotenoids, inhibited activity of photosystem II, and affected cell sizes. A stereochemical analog of glucose, 2-deoxy-D-glucose, induced effects similar to those of glucose. A comparison with the effects of red and green light demonstrated that glucose acted on Calothrix similarly to red light and oppositely to green light.Translated from Fiziologiya Rastenii, Vol. 52, No. 2, 2005, pp. 266–273.Original Russian Text Copyright © 2005 by Lebedeva, Boichenko, Semenova, Pronina, Stadnichuk.This revised version was published online in April 2005 with a corrected cover date.     

A New Appraisal of the Prokaryotic Origin of Eukaryotic Phytochromes

The evolutionary origin of the phytochromes of eukaryotes is controversial. Three cyanobacterial proteins have been described as ``phytochrome-like' and have been suggested to be potential ancestors of these essential photoreceptors: Cph1 from Synechocystis PCC 6803, showing homology to phytochromes along its entire length and known to attach a chromophore; and PlpA from Synechocystis PCC 6803 and RcaE from Fremyella diplosiphon, both showing homology to phytochromes most strongly only in the C-terminal region and not known to bind a chromophore. We have reexamined the evolution of the photoreceptors using for PCR amplification a highly conserved region encoding the chromophore-binding domain in both Cph1 and phytochromes of plants and have identified genes for phytochrome-like proteins (PLP) in 11 very diverse cyanobacteria. The predicted gene products contain either a Cys, Arg, Ile, or Leu residue at the putative chromophore binding site. In 10 of the strains examined only a single gene was found, but in Calothrix PCC 7601 two genes (cphA and cphB) were identified. Phylogenetic analysis revealed that genes encoding PLP are homologues that share a common ancestor with the phytochromes of eukaryotes and diverged before the latter. In contrast, the putative sensory/regulatory proteins, including PlpA and RcaE, that lack a part of the chromophore lyase domain essential for chromophore attachment on the apophytochrome, are only distantly related to phytochromes. The Ppr protein of the anoxygenic photosynthetic bacterium Rhodospirillum centenum and the bacterial phytochrome-like proteins (BphP) of Deinococcus radiodurans and Pseudomonas aeruginosa fall within the cluster of cyanobacterial phytochromes. Received: 9 December 1999 / Accepted: 10 May 2000     

Chromatic adaptation and photoreversal in blue-green algaCalothrix clavata West

Complementary chromatic adaptation, a well-established phenomenon in some blue-green algae, has been observed inCalothrix clavata, a heterocystous blue-green alga of the family Rivulariaceae. The chromatic adaptation has been observed for fluorescent and incandescent light by measuring the absorption spectra. The material grown in fluorescent light forms more of phycoerythrin whereas more of phycocyanin tends to be formed in incandescent light. Besides this, photoreversal was observed by transferring the incandescent light grown alga to fluorescent light conditions and vice-versa. Effect of photoreversal and chromatic adaptation has also been discussed for this alga under different monochromatic light conditions. The influence of different light conditions on morphological changes, heterocysts and hormogonia formation has also been investigated. Both chromatic adaptation and photomorphogentic phenolmena in this alga show the involvement of some photoreversible (red:green) pigment.     

Lesions in phycoerythrin chromophore biosynthesis in Fremyella diplosiphon reveal coordinated light regulation of apoprotein and pigment biosynthetic enzyme gene expression

We have characterized the regulation of the expression of the pebAB operon, which encodes the enzymes required for phycoerythrobilin synthesis in the filamentous cyanobacterium Fremyella diplosiphon. The expression of the pebAB operon was found to be regulated during complementary chromatic adaptation, the system that controls the light responsiveness of genes that encode several light-harvesting proteins in F. diplosiphon. Our analyses of pebA mutants demonstrated that although the levels of phycoerythrin and its associated linker proteins decreased in the absence of phycoerythrobilin, there was no significant modulation of the expression of pebAB and the genes that encode phycoerythrin. Instead, regulation of the expression of these genes is coordinated at the level of RNA accumulation by the recently discovered activator CpeR.     

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.     

Phosphorelay control of phycobilisome biogenesis during complementary chromatic adaptation

For some cyanobacteria, the spectral distribution of light in the environment regulates the synthesis of specific polypeptides of the phycobilisome or light harvesting antenna complex. This process, called complementary chromatic adaptation, is controlled by a complex type of two component regulatory system. In such pathways, phosphorelay typically occurs through two histidine and two aspartate residues. Generation and complementation of mutants in CCA have uncovered three elements of this pathway, a putative sensor, RcaE, and two response regulators, RcaC and RcaF. RcaC, a large response regulator, contains two input domains, a DNA binding motif and a putative histidine phosphoacceptor domain. RcaF is a small response regulator and apparently lacks an output domain. Ordering of the pathway components has placed RcaE before RcaF, and RcaF before RcaC. This phosphorelay circuitry is novel because it has, instead of four, at least five potential phosphoacceptor domains for signal transduction.     

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

Changes 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.     

Chromatic adaptation in a mutant of Fremyella diplosiphon incapable of phycoerythrin synthesis

A mutant of the chromatically adapting cyanobacterium Fremyella diplosiphon, incapable of phycoerythrin synthesis but responding to wavelength modulation of its biliprotein content, was isolated. The biliprotein composition of the mutant and of the wild type were identical after growth in red light, but green light induced, in the mutant, the synthesis of a biliviolin-type chromophore bound to some of the alpha subunits of its phycocyanin. Implications of the results on the regulation and possible pathways of biliprotein biosynthesis are discussed.