Tracking the Light Environment by Cyanobacteria and the Dynamic Nature of Light Harvesting

In nature photosynthetic organisms cope with fluctuating light conditions. Light intensity and quality vary dramatically during the day or from one habitat to another. Photosynthetic organisms sense intensities and wavelengths of light both directly and indirectly. Because light fuels photosynthetic electron transport and CO2 fixation, it is the primary determinant of levels of NADP/NADPH, ATP, and carbon metabolites, all of which can serve to modulate cellular processes. Light is also absorbed by photoreceptors that link light cues to cellular metabolism. However, light represents a single environmental cue, and other signals interact with light through a web of regulatory circuits that result in dynamic acclimatory responses. This review focuses on two specific aspects of light-influenced processes in Cyanobacteria; both concern changes in light harvesting structure and biosynthesis. The first part of this review discusses effects of changing wavelengths of light on the biosynthesis of the phycobilisomes (PBS),1 dominant light harvesting complexes of Cyanobacteria. The other discusses how Cyanobacteria tune light harvesting and photosynthetic function to both light intensity and nutrient availability and how the two responses are integrated. PBS are peripheral membrane complexes in Cyanobacteria that efficiently harvest light energy and transfer the energy to photosynthetic reaction centers. PBS, which can comprise 30% of the cellular protein, are organized into two structural domains, the core and rods (Fig. 1). Each of these domains contains pigmented and nonpigmented polypeptides. All PBS have the chromoproteins (phycobiliproteins) allophycocyanin (AP) and phycocyanin (PC), and many also contain phycoerythrin (PE) or phycoerythrocyanin. Phycobiliprotein colors are a consequence of light absorption by linear tetrapyrrole chromophores that covalently associate with the apoproteins ( 1The abbreviations used are:PBSphycobilisome(s)APallophycocyaninPCphycocyaninPEphycoerythrinL polypeptidelinker polypeptideCCAcomplementary chromatic adaptationRLred lightGLgreen lightHLhigh lightPASPER/ARNT/SIMDCMU3-(3,4-dichlorophenyl)-1, 1-dimethylureaDBMIB2,5-Dibromo-3-methyl-6-isopropyl-p-benzoquinone, 2Glazer A.N. Lundell D.J. Yamanaka G. Williams R.C. Ann. Microbiol (Inst. Pasteur). 1983; 134B: 159-180Crossref Scopus (79) Google Scholar). Phycobiliproteins are composed of α and β subunits associated into heterodimers (termed “monomers” in the literature) that aggregate into trimers (αβ)3 and hexamers (αβ)6. Nonchromophorylated linker (L) polypeptides stabilize PBS, facilitate assembly of phycobiliprotein aggregates, and modulate the absorption characteristics of phycobiliproteins, promoting unidirectional energy flow to photosynthetic reaction centers (1Glazer A.N. Annu. Rev. Biophys. Biophys. Chem. 1985; 14: 47-77Crossref PubMed Scopus (445) Google Scholar). phycobilisome(s) allophycocyanin phycocyanin phycoerythrin linker polypeptide complementary chromatic adaptation red light green light high light PER/ARNT/SIM 3-(3,4-dichlorophenyl)-1, 1-dimethylurea 2,5-Dibromo-3-methyl-6-isopropyl-p-benzoquinone PBS cores contain AP trimers along with pigmented and L polypeptides. A high molecular mass core polypeptide, or LCM, has homology to both phycobiliproteins and L polypeptides (3Capuano V. Braux A.-S. Tandeau de Marsac N. Houmard J. J. Biol. Chem. 1991; 266: 7239-7247Abstract Full Text PDF PubMed Google Scholar). The phycobiliprotein-like domain of LCM binds a tetrapyrrole chromophore and can serve as a PBS terminal energy acceptor. Generally, six rods, each composed of stacks of PC and PE hexamers, radiate from the core, giving PBS a fanlike appearance (Fig. 1) (see Ref. 2Glazer A.N. Lundell D.J. Yamanaka G. Williams R.C. Ann. Microbiol (Inst. Pasteur). 1983; 134B: 159-180Crossref Scopus (79) Google Scholar for details). It was noted over a century ago that Cyanobacteria pigmentation changes with environmental light quality. This light control of pigmentation, shown in the lower half of Fig. 1, was termed complementary chromatic adaptation (CCA). Bennett and Bogorad (4Bennett A. Bogorad L. J. Cell Biol. 1973; 58: 419-435Crossref PubMed Scopus (1100) Google Scholar) showed that CCA was the result of altered PBS pigment-protein composition. Development of molecular tools in the 1970s created new opportunities for elucidating PBS regulation, and by the end of the 1980s most genes encoding PBS structural polypeptides were characterized (5Tandeau de Marsac N. Houmard J. FEMS Microbiol. Rev. 1993; 104: 119-190Crossref Google Scholar). In the Cyanobacterium Fremyella diplosiphon (similar to Calothrix PCC7601) the PE:PC ratio reflects the spectral distribution of light in the environment (6Bryant D.A. Cohen-Bazire G. Eur. J. Biochem. 1981; 119: 415-424Crossref PubMed Scopus (46) Google Scholar). In red light (RL) the organism has almost no PE, and each PBS rod can have three PC hexamers (and specific L polypeptides). If the Cyanobacterium is moved to green light (GL), new PBS are synthesized with rods having single PC hexamers (core proximal hexamer) and up to three PE hexamers. As the cells replicate in GL, blue-pigmented PBS of RL-grown cells are gradually diluted, and the cells begin to appear red. These light-responsive changes are reversible, and because PC absorbs RL (λmax = 620 nm) and PE absorbs GL (λmax = 560 nm), these changes facilitate efficient absorption of prevalent wavelengths of light in the environment. Knowledge of genes encoding phycobiliprotein and linker polypeptide has been critical for understanding CCA (see Refs. 5Tandeau de Marsac N. Houmard J. FEMS Microbiol. Rev. 1993; 104: 119-190Crossref Google Scholar and 7Grossman A.R. Kehoe D.M. Photosynth. Res. 1997; 53: 95-108Crossref Google Scholar)). Genes encoding α and β subunits of each phycobiliprotein are contiguous on the cyanobacterial genome and are cotranscribed. Often, polycistronic transcripts encode phycobiliprotein subunits and their associated L polypeptides. In F. diplosiphon, α and β AP subunits (αAP and βAP, respectively), encoded by the apcA1B1 genes, are in an operon that also contains the apcC1 and apcE1 genes; the latter genes encode the core linker polypeptide and the LCM, respectively (8Houmard J. Capuano V. Cousin T. Tandeau de Marsac N. J. Bacteriol. 1988; 170: 5512-5521Crossref PubMed Google Scholar). Three distinct operons encode αPC and βPCsubunits (cpcBA genes) in F. diplosiphon (9Conley P.B. Lemaux P.G. Grossman A.R. Science. 1985; 230: 550-553Crossref PubMed Scopus (57) Google Scholar, 10Conley P.B. Lemaux P.G. Lomax T.L. Grossman A.R. Proc. Natl. Acad. Sci. U. S. A. 1986; 83: 3924-3928Crossref PubMed Scopus (42) Google Scholar, 11Mazel D. Houmard J. Tandeau de Marsac N. Mol. Gen. Genet. 1988; 211: 296-304Crossref PubMed Scopus (65) Google Scholar, 12Mazel D. Marliere P. Nature. 1989; 341: 245-248Crossref PubMed Scopus (123) Google Scholar). The cpcB1A1 genes are constitutively transcribed and encode PCc subunits (subscript indicatesconstitutive). This operon also contains cpcEand cpcF, which encode a lyase that attaches the tetrapyrrole chromophores to the α subunit of PC (13Fairchild C.D. Glazer A.N. J. Biol. Chem. 1994; 269: 8686-8694Abstract Full Text PDF PubMed Google Scholar). ThecpcB2A2 operon is specifically active in RL (inactive in GL) and encodes PCi (subscript indicatesinducible), which is critical for CCA. Hexamers of PCi comprise the majority of PBS rods when cyanobacterial cells are grown in RL. The genes cpcH2, cpcI2,and cpcD2 (14Lomax T.L. Conley P.B. Schilling J. Grossman A.R. J. Bacteriol. 1987; 169: 2675-2684Crossref PubMed Google Scholar), encoding L polypeptides associated with PCi, are cotranscribed with cpcB2A2. Furthermore, the cpcB2A2H2I2D2 operon is clustered on theF. diplosiphon genome with cpcB1A1 andapcE1A1B1C1 (10Conley P.B. Lemaux P.G. Lomax T.L. Grossman A.R. Proc. Natl. Acad. Sci. U. S. A. 1986; 83: 3924-3928Crossref PubMed Scopus (42) Google Scholar). A third PC operon, cpcB3A3 plus genes encoding associated L polypeptides, is only active during sulfur-limited growth (12Mazel D. Marliere P. Nature. 1989; 341: 245-248Crossref PubMed Scopus (123) Google Scholar). The cpeBA operon encodes α and β subunits of PE (15Mazel D. Guglielmi G. Houmard H. Sidler W. Bryant D.A. Tandeau de Marsac N. Nucleic Acids Res. 1986; 14: 8279-8290Crossref PubMed Scopus (93) Google Scholar). In contrast to the situation for cpc and apcoperons, genes encoding L polypeptides associated with PE are not contiguous on the genome to cpeBA; they are encoded by thecpeCDE operon (16Federspiel N.A. Scott L. J. Bacteriol. 1992; 179: 5994-5998Crossref Google Scholar). However, GL activation and RL suppression of cpeBA and cpeCDE are coordinated. Also, cpeBA genes are linked to cpeY andcpeZ, which encode the lyase that attaches tetrapyrrole chromophores to PE subunits (17Kahn K. Mazel D. Houmard J. Tandeau de Marsac N. Schaefer M.R. J. Bacteriol. 1997; 179: 998-1006Crossref PubMed Google Scholar). Action spectra for the synthesis of PC and PE in the Cyanobacteria have been measured (18Vogelmann T.C. Scheibe J. Planta. 1978; 143: 233-239Crossref PubMed Scopus (54) Google Scholar). Maximum PE synthesis and minimum PC synthesis occurred following exposure to 550 nm GL, and maximal PC synthesis and minimal PE synthesis occurred following exposure to 640 nm RL. Hence, photoreceptor(s) controlling CCA absorb RL and GL but elicit different responses in the two light qualities. PC synthesis dominates in RL whereas PE synthesis dominates in GL. Exposure of cells to natural sunlight, a mixture of RL and GL, results in the synthesis of PBS with intermediate PC and PE levels. Photocontrol of PE and PCi levels is primarily a consequence of transcriptional regulation of cpeBA andcpcB2A2 operons (19Casey E.S. Grossman A.R. J. Bacteriol. 1994; 176: 6362-6374Crossref PubMed Google Scholar, 20Schmidt-Goff C.M. Federspiel N.A. J. Bacteriol. 1993; 175: 1806-1813Crossref PubMed Google Scholar, 21Sobczyk A. Schyns G. Tandeau de Marsac N. Houmard J. EMBO J. 1993; 12: 997-1004Crossref PubMed Scopus (47) Google Scholar). The dissection of regulatory circuits involving CCA has exploited mutants abnormal for CCA. Several classes of CCA mutants have been isolated (5Tandeau de Marsac N. Houmard J. FEMS Microbiol. Rev. 1993; 104: 119-190Crossref Google Scholar, 22Bruns B. Briggs W.R. Grossman A.R. J. Bacteriol. 1989; 171: 901-908Crossref PubMed Google Scholar, 23Cobley J.G. Miranda R.D. J. Bacteriol. 1983; 153: 1486-1492Crossref PubMed Google Scholar, 24Kehoe D.M. Grossman A.R. Science. 1996; 273: 1409-1412Crossref PubMed Scopus (312) Google Scholar), including the red (FdR), blue (FdB), green (FdG), and black (FdBk) strains. FdR mutants are red under all conditions of illumination and constitutively synthesize PE whereas PCi is never synthesized. These mutants are fixed in a response normally exhibited only in GL, with aberrant regulation of both the cpeBA and cpcB2A2 operons (22Bruns B. Briggs W.R. Grossman A.R. J. Bacteriol. 1989; 171: 901-908Crossref PubMed Google Scholar). FdB strains are bluer than wild-type cells in RL and require more GL to suppress PCi synthesis (25Casey E.S. Kehoe D.M. Grossman A.R. J. Bacteriol. 1997; 179: 4599-4606Crossref PubMed Google Scholar). FdG mutants show normal PCi expression, but the cpeBA genes never become active. FdBk mutants have moderate levels of both PE and PCi, which remain the same in RL and GL (7Grossman A.R. Kehoe D.M. Photosynth. Res. 1997; 53: 95-108Crossref Google Scholar, 24Kehoe D.M. Grossman A.R. Science. 1996; 273: 1409-1412Crossref PubMed Scopus (312) Google Scholar). Initially, an FdR mutant was complemented by rcaC, which encodes a polypeptide of 651 amino acids with sequence similarities to response regulators of two-component regulatory systems (26Chiang G.G. Schaefer M.R. Grossman A.R. Proc. Natl. Acad. Sci. U. S. A. 1992; 89: 9415-9419Crossref PubMed Scopus (67) Google Scholar). It is twice as large (73 kDa) as most response regulators and has two conserved, aspartate-containing receiver domains, one at the N terminus (Asp-51) and the other at the C terminus (Asp-576). The Asp-51 residue is likely phosphorylated in RL-grown cells, and the phosphorylation results in high level PCi and little PE synthesis. In GL wild-type cells likely dephosphorylate Asp-51, which triggers elevated PE synthesis and depressed PCi synthesis. Contiguous to the N-terminal receiver domain of RcaC is a sequence predicted to bind DNA. Between the putative DNA binding domain and the C-terminal receiver domain is a motif that resembles an H block of some unorthodox sensor proteins (27Appleby J.L. Parkinson J.S. Bourret R.B. Cell. 1996; 86: 845-848Abstract Full Text Full Text PDF PubMed Scopus (344) Google Scholar). The FdBk class of mutants was complemented by rcaE, which encodes a polypeptide of 74 kDa (24Kehoe D.M. Grossman A.R. Science. 1996; 273: 1409-1412Crossref PubMed Scopus (312) Google Scholar). The C-terminal region of RcaE has motifs typical of bacterial sensor kinases (with a typical H block). The N-terminal half of the polypeptide has a domain of about 140 amino acids with similarity to the tetrapyrrole chromophore attachment domain of phytochromes. The central region of the protein contains a PAS domain (28Taylor B.L. Zhulin I.B. Microbiol. Mol. Biol. Rev. 1999; 63: 479-506Crossref PubMed Google Scholar), which may be involved in protein-protein interactions or binding of a redox-active prosthetic group. Recently RcaE was shown to covalently bind a linear tetrapyrrole chromophore at a cysteine within the phytochrome-like domain. 2D. M. Kehoe and A. R. Grossman, unpublished data. The phenotype of the FdBk mutant and similarity of RcaE to sensor kinases and eukaryotic phytochrome photoreceptors are consistent with a photoreceptor role for RcaE (7Grossman A.R. Kehoe D.M. Photosynth. Res. 1997; 53: 95-108Crossref Google Scholar, 24Kehoe D.M. Grossman A.R. Science. 1996; 273: 1409-1412Crossref PubMed Scopus (312) Google Scholar). Two FdR mutants were not complemented by rcaC (29Kehoe D.M. Grossman A.R. J. Bacteriol. 1997; 179: 3914-3921Crossref PubMed Scopus (84) Google Scholar). One was complemented by the putative photoreceptor gene rcaE, and the second by rcaF, which is immediately downstream ofrcaE on the F. diplosiphon genome and encodes a small response regulator. RcaF may act as an intermediate in the phosphorelay pathway controlling CCA and facilitate phosphate transfer from its cognate sensor (presumably RcaE) to other response regulators such as RcaC. Because rcaE is sufficient for complementing both FdBk (24Kehoe D.M. Grossman A.R. Science. 1996; 273: 1409-1412Crossref PubMed Scopus (312) Google Scholar) and FdR mutants, different lesions in rcaE can generate different phenotypes. Furthermore, an FdR phenotype can result from lesions in at least three distinct genes (rcaC,rcaE, and rcaF). The lesions that caused the mutant phenotype in these strains were the result of gene disruption byin vivo transposition (22Bruns B. Briggs W.R. Grossman A.R. J. Bacteriol. 1989; 171: 901-908Crossref PubMed Google Scholar). Each of the FdBk (rcaE-FdBk) and FdR (rcaE-FdR,rcaF-FdR) mutants characterized contained insertion sequences in the rcaE/rcaF operon (29Kehoe D.M. Grossman A.R. J. Bacteriol. 1997; 179: 3914-3921Crossref PubMed Scopus (84) Google Scholar). InrcaE-FdBk mutants the inserts were located within 200 base pairs of the putative translation start site, and no RcaE protein was detected in mutant cells.2 The rcaE-FdR mutants contained insertions positioned between the H block and the four conserved motifs critical for histidine kinase activity; this strain appears to synthesize truncated RcaE. The rcaF-FdR mutants contained insertions located ∼200 base pairs downstream of thercaF translation initiation codon. Constitutive PE and PC synthesis in rcaE-FdBk mutants reflect an intermediate activation state of the system as a consequence of level phosphorylation of regulatory that are no under RcaE Hence, RcaF likely level phosphorylation in the of this phosphorylation is not by light quality and may result from between RcaF and other or transfer from small It is not that a in a sensor kinase to an activation of the phosphorelay In the rcaE-FdR mutants, the truncated RcaE it may bind RcaF and block its phosphorylation by other which RcaF in a Three regulatory critical for CCA are and RcaC. these polypeptides have of bacterial two-component the CCA phosphorelay is because it domains these polypeptides. the putative the light RL RcaE to an by transfer of the to the response In the of RcaF may interact with other RcaF may transfer to the conserved histidine of the H block within which can it to the or C-terminal receiver domain. The N-terminal receiver domain of RcaC is critical for whereas the role of the C-terminal receiver domain is In GL RcaE as a or by binding to this activation of cpeBA and suppression other regulatory also appear to be involved in controlling CCA. A class of mutants that only has been and is These mutants normal regulation but cpeBA in GL. of the strains two and encoding polypeptides to protein M. this is because phosphorylation of the putative regulatory protein has been in the control A. Schyns G. Tandeau de Marsac N. Houmard J. EMBO J. 1993; 12: 997-1004Crossref PubMed Scopus (47) Google Scholar). of organisms to nutrient availability may be as specific to the nutrient and that are more during of a of different nutrient conditions. responses changes organisms to efficiently the these responses may synthesis of high transport systems Grossman A.R. J. Bacteriol. 1988; 170: PubMed Google Scholar) and of that facilitate of of the nutrient D. Grossman A.R. J. 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EMBO J. 1994; PubMed Scopus Google may be the primary gene be elevated to during or is not a it may function to or the of a or PBS for A second mutant was complemented by has homology to subunits of that attachment of chromophores to subunits N. Grossman A.R. J. Bacteriol. 1999; PubMed Google Scholar). This that directly with tetrapyrrole chromophores to Because mutants not PBS during nutrient it is to that of chromophores from subunits and that only the chromophore is can phycobiliprotein subunits be A third was complemented by a gene encoding a response R. Grossman A.R. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar). Cyanobacteria strains for have the level of PBS as wild-type cells during to PBS during or and modulate PBS levels during exposure to high light The and reflect the that the mutant during nutrient The mutant also when for or or when to R. Grossman A.R. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar). Hence, in to controlling PBS critical for during and conditions. The of the photosynthetic electron transport the of the during and that of the mutant is a consequence of its to exposure to conditions. Hence, appears to have a role in some responses and is critical for environmental signals with cellular metabolism. The most characterized mutant the mutant is to and nutrient and Furthermore, the strain encoding a polypeptide with similarity to and proteins of that Cyanobacteria to N. Grossman A.R. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google and during exposure to or N. and A. R. Grossman, for is also for the of the genes in The gene encodes a sensor histidine kinase of two-component regulatory with two predicted N-terminal domains by a region a PAS domain. PAS domains bind or prosthetic and may to light or conditions (28Taylor B.L. Zhulin I.B. Microbiol. Mol. Biol. Rev. 1999; 63: 479-506Crossref PubMed Google Scholar). that binds a L. W. and A. R. Grossman, unpublished data. Because nutrient responses and of that and a this has not been of in not appear to be under the control that regulatory that are distinct from by the results that to link the light environment and cellular to of processes. The of light and nutrient responses are in Fig. is critical for these which of PBS levels and controlling the of and It is not is critical for of other genes that to changes in light conditions. nutrient as cells generate photosynthetic electron a phosphorylation in which is on and in with also other processes in the of the photosynthetic that during nutrient and conditions. the of many genes encoding of the photosynthetic of a of these genes not require Hence, in to with associate with other response regulators that have not been A is how may be the state of the nutrient when the of the is or the electron of the photosynthetic electron transport is not as as under conditions and the electron are in a under conditions the electron may be than they are nutrient and result in absorption of light energy by photosynthetic and the cellular environment become The state of photosynthetic electron is to modulate cellular M. J. P.G. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar), translation J. Science. 1997; PubMed Scopus Google Scholar), state and changes in the of the N. M. S. The Scholar). The results that control is linked to the state of the cells and to the of of specific photosynthetic electron Furthermore, both which photosynthetic electron flow and which electron flow through the PBS and the of during and PBS and expression, of is altered by both and of with both and photosynthetic electron flow at is in in a mutant of is elevated of genes in moderate These results that of an electron transport to may during and nutrient conditions. in to the state of the photosynthetic may be for the of control to PBS during nutrient but in it control activation with a blue light photoreceptor or the absorption of light by may also regulatory pathway over may also serve as regulatory signals that modulate the of the Several aspects of the are However, it represents an that effects in response to of photosynthetic electron and nutrient growth and light to regulation of cellular metabolism.