Département de Biologie Joliot-Curie, SBFM, CEA Saclay, F-91191, Gif-sur-Yvette, France
Correspondence
Ghada Ajlani
gajlani{at}cea.fr
![]() |
ABSTRACT |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Present address: Institute of Plant Biology, BRC, Temesvári Krt. 62, H-6701, Szeged, Hungary.
![]() |
INTRODUCTION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
As the PBSs in cyanobacteria constitute a substantial fraction of the total soluble proteins (50 %), their degradation can supply amino acids for the synthesis of essential proteins under nutrient-limited conditions (Allen & Smith, 1969). Indeed, the PBS is degraded in a specific and orderly manner during nitrogen starvation of non-diazotrophic cyanobacteria (Yamanaka & Glazer, 1980
). This process, known as bleaching or PBS trimming, requires the nblA gene, which is induced and necessary for PBS trimming under nitrogen starvation (Collier & Grossman, 1994
; Luque et al., 2003
). During PBS trimming, PC hexamers and associated linkers most distal to the core are degraded first (Richaud et al., 2001
; Yamanaka & Glazer, 1980
). Another type of PBS trimming occurs under high-light conditions and does not involve nblA (Collier & Grossman, 1994
; Garnier et al., 1994
; Lönneborg et al., 1985
).
PBSs are not required for phototrophic growth (Ajlani & Vernotte, 1998; Bruce et al., 1989
) so mutations affecting different linkers are of special interest because they provide the opportunity for observing PBS biogenesis in normal growth conditions. Understanding PBS assembly has been enhanced by mutational analysis of Synechococcus sp. strain PCC7002, but this strain contains only two PC hexamers and two linkers per rod. The phycobilisome of Synechocystis sp. strain PCC6803 consists of a three-cylindrical core from which six rods radiate, each rod being composed of three stacked PC hexamers and three rod linkers (Elmorjani et al., 1986
). Most of the rod-subunit-encoding genes are clustered in the cpc operon. In Synechocystis sp. strain PCC6803, this operon contains five genes: cpcB and cpcA encode the
PC and
PC subunits, respectively, while cpcC2, cpcC1 and cpcD encode the rod linkers
,
and
, respectively. Two independent genes (cpcG1 and cpcG2) encode the rod-core linker (LRC) that attaches the proximal PC hexamer to the core (Cyanobase: http://www.kazusa.or.jp/cyano/Synechocystis/).
Using interposon mutagenesis, we have constructed and characterized deletion mutants in the three rod-linker genes located in the cpc operon of Synechocystis sp. strain PCC6803. Characterization of the PBS assembly process in the mutants yielded a scheme for PBS-rod biogenesis in Synechocystis sp. strain PCC6803 in which the insertion of is excluded in the absence of
. This result differs from studies with mutants of Synechococcus sp. strain PCC7942 lacking rod-linker genes, in which it has been proposed that
and
could occupy interchangeable positions within the rods (Bhalerao et al., 1991
, 1993
).
We demonstrated, by monitoring steady-state RNA levels in the mutants, that the cassette insertion affected gene expression in its vicinity, regardless of orientation. This polar effect provided us with strains containing different levels of the rod linkers, and whose absorption spectra showed that the PC level incorporated in the PBS varied proportionally. This result leads to the proposal that transcriptional regulation of the rod-linker genes adjusts the light-harvesting capacity of the photosynthetic apparatus by modulating the PBS rod length.
![]() |
METHODS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
Construction of plasmids and mutants.
Primers pcf and pcr (5'-GTAGGCTGTGGTTCCCTAG-3' and 5'-CACACTCTCAACGGTTCCG-3', respectively) were used for the PCR amplification of the cpc operon from Synechocystis sp. strain PCC6803 total DNA. Primers were designed according to the Cyanobase complete genome sequence. The 4·2 kb PCR product was digested with MfeI and PstI and cloned into EcoRI- and PstI-digested pUC9. The resulting plasmid, denoted pCPC, carried a 4 kb fragment which contained the five genes of the cpc operon plus 480 bp upstream of the cpcB start codon and 260 bp downstream from the stop codon of the last gene, cpcD. Part or all of cpcC2 and cpcC1 were substituted by the Km cassette in the inactivation plasmids pC30K+, pC30K, pC33K+ and pCBK+ (Table 1). Mutants 30f, 30r, 33 and CB were created by transformation of the wild-type Synechocystis sp. strain PCC6803 with each of these plasmids, respectively, followed by screening for Kmr colonies. p
C2
was constructed starting from an EagI-digested pCPC plasmid treated for 20 min with BAL31 nuclease, then SpeI digested, treated with the Klenow DNA polymerase and ligated; the resulting plasmid contained a 685 bp deletion in cpcC2. Subsequently, the
cartridge was inserted in the BseRI site. Transforming CB and the wild-type with plasmid p
C2
and screening for (Kms, Spr) colonies resulted in
30D3 and D3, respectively. Transformation of the wild-type with pUCD
and screening for Spr colonies gave the D4 mutant. For trans-complementations of cpcC1 and cpcD, pS1C1 and pS1D were respectively used to transform the appropriate strains (Table 1
). pS1D was constructed to express cpcD from the psbAII promoter by inserting into pPSBA2 a 380 bp NdeIBamHI fragment containing cpcD plus a BamHI fragment carrying the aphI gene (Fig. 1
). The cpcD-containing fragment was amplified using the following oligonucleotides: fd (5'-GAATTCCATATGTTAGGTCAATCTTC-3') and rd (5'-GGGATCCTGACTCGATGGCTATTC-3'). NdeI and BamHI sites are underlined. pS1C1 was constructed to express cpcC1 from the psbAII promoter by inserting a 3·3 kb HincII fragment from 30 bp upstream of the cpcC1 start codon (containing the ribosome-binding site) to 35 bp downstream of the cpcC1 stop codon plus the
cassette in pPSBA2 (Fig. 1
).
|
PBS isolation and analysis.
Cells were broken by vortexing with glass beads. Phycobilisomes were prepared from Synechocystis sp. strain PCC6803 as described by Ajlani et al. (1995) and Glazer (1988)
. Absorption spectra were recorded on a Varian Cary-5E double-beam spectrophotometer, with a data interval of 0·5 nm. Proteins were analysed by SDS-PAGE on a 1020 % linear polyacrylamide gradient in a modified Tris/glycine buffer (Fling & Gregerson, 1986
) or 412 % Bis-Tris gels (NuPAGE, Novex) in MES-SDS buffer. OD at 620 nm was used to ensure approximately equal loading of different PBS samples; about 0·3 OD620 ml (100 µl from a sample at OD620=3) was loaded per well. PBS-containing samples were concentrated by precipitation with 10 % (w/v) trichloroacetic acid prior to loading. Proteins were visualized using Coomassie Brilliant Blue stain.
![]() |
RESULTS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The PBSs from each of the mutants were purified in order to determine their polypeptide composition. Sucrose gradients from all the PBS preparations contained a dark-blue band in the 1 M sucrose layer at positions near those expected for a complete PBS, indicating that PBSs were assembled. However, the assembled particles were at slightly higher positions on the sucrose gradient than those of the wild-type and the D3 strain, which indicated that the absence of resulted in the assembly of a smaller PBS. The reduction of the PBS size is accompanied by the appearance of a free PC band at the top of the gradient tubes in the 0·25 M sucrose layer, indicating that a certain amount of synthesized PC is not incorporated into rods. Less free PC was found in 30r than in 30f and
30D3. Fluorescence emission upon excitation with biliprotein-sensitizing light showed high emission from PC in cpcC2-deficient cells compared to the wild-type and D3, confirming the presence of unincorporated PC in these strains (data not shown).
The polypeptide composition of purified PBSs from the mutants was analysed by Coomassie-stained SDS-PAGE. In addition to the phycobiliproteins (PC and AP) in the 20 kDa range, wild-type PBSs contain seven polypeptides (Fig. 2a, lane WT). Four of these polypeptides, not encoded by the cpc operon, were invariably present in all strains: LC, core linker; LRC, rod-core linker; FNR, Ferredoxin NADP+ Reductase and LCM, core-membrane linker. As expected, the
polypeptide was absent from the three cpcC2-deleted strains,
30D3, 30f and 30r. At the same time, these strains exhibited decreasing amounts of the
polypeptide (traces, if any, in 30r) (Fig. 2a
). The
polypeptide was detected only in the 30f PBS, albeit in lesser amount than in the wild-type PBS.
|
The steady-state level of cpc transcripts was monitored in the mutants by Northern blot. The wild-type operon specifies three differently sized mRNAs which start upstream of the translation initiation codon of cpcB and terminate at three different sites (Fig. 3a). The smaller and most abundant transcript (1·6 kb), containing cpcB and cpcA, does not seem to be affected in any of the mutants (Fig. 3b
, panel 1). Two larger and less-abundant transcripts, which contain the linker-encoding genes cpcC2, cpcC1 and cpcD, are detected at 3·4 and 3·8 kb in the wild-type (Fig. 3b
, panels 1 and 2, lane WT). The size and relative abundance of these transcripts are changed in the mutants. In the 30r and 30f strains, they would be about 0·6 kb larger due to the deletion in cpcC2 and the Km cassette insertion; their sizes should be 4·0 and 4·4 kb, respectively. They were undetectable in the 30r strain and present in a drastically reduced amount in strain 30f (Fig. 3b
, panel 2). In D3, the 3·8 kb transcript is absent due to the strong transcription terminators present in
, while the 3·4 kb transcript seems less abundant than in the wild-type. This might be due to a stemloop disturbed by the
insertion (see Discussion). In
30D3, a shorter form of this transcript (2·7 kb due to the deletion in cpcC2) is detected and seems fairly abundant. The blot was hybridized with a Km probe and overexposed to detect mRNAs containing the Km cassette (Fig. 3b
, panel K). In 30f, two major transcripts are detected at 4·0 and 2·9 kb, while in strain 30r, the 4·0 kb one was barely detectable and the 2·0 kb transcript that also hybridized to probe 1 was obvious. Larger bands (around 2·5 kb) could be the products of abortive transcription and degradation of the full operon transcript. The 4·0 kb transcripts correspond to the transcription of the whole operon through the Km cassette. Their low amounts demonstrate that the insertion of the Km cassette destabilizes those transcripts. The 2·9 and 2·0 kb transcripts, in 30f and 30r, respectively, are the products of readthrough transcription from the aphI promoter. The 2·9 kb transcript detected in 30f terminates at the end of the cpc operon: it should then contribute to the translation of cpcC1 and cpcD. The size of the 2 kb transcript in 30r implies that it terminates within cpcB. Part of this transcript is an antisense RNA to the 1·6 kb mRNA containing cpcB and cpcA.
|
Sucrose gradients of PBS preparations from 33 and CB contained a dark-blue band at a position significantly higher on the gradient than those of the wild-type PBS, indicating that assembled PBSs were much smaller in size. Again, free PC bands at the top of the gradients indicate the presence of unincorporated PC in the cells. The SDS-PAGE of purified PBSs showed no trace of either or
in CB. More surprisingly, both linkers were also absent in strain 33. The relative amounts of
were also significantly reduced in both mutants (Fig. 4a
, lanes 33 and CB). PBSs from 33 and CB have identical absorption spectra, similar to the spectrum of 30r (Fig. 4b
). The absence of
in the PBS from strain 33 suggests that
was not incorporated into the PBS in the absence of
. In order to corroborate this hypothesis and to exclude any polar effect of the cpcC1 mutation, both CB and 33 were complemented with a transcriptional fusion in which cpcC1 was placed under the control of the strong psbAII promoter in the psbAII locus (Fig. 1
, pS1C1). The resulting strains were denoted CBc and 33c, respectively. This insertion is neutral to Synechocystis sp. strain PCC6803, since it has been shown that psbAIII can support photoautotrophic growth in the absence of psbAII (Mohamed & Jansson, 1989
). The SDS-PAGE showed that CBc PBSs recovered
, demonstrating that the ectopic cpcC1 gene was expressed and capable of complementing the deleted gene. PBSs from 33c recovered both
and
, confirming that the absence of both linkers in 33 was due only to the deletion of cpcC1 (Fig. 4a
). Absorption spectra showed increased amounts of PC in CBc and 33c PBSs compared to their parent mutants CB and 33, respectively. The extent of this increase was more spectacular in 33c, since it recovered two rod linkers and their associated PC (Fig. 4b
). These results prove that cpcC2 was functional in strain 33; the absence of its product,
, in the PBS was due to an epistatic effect of cpcC1 on cpcC2. It is noteworthy that the relative amounts of
also increased in the PBSs of 33c compared to CB, CBc and 33 (Fig. 4a
).
|
|
![]() |
DISCUSSION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The three allelic cpcC2 mutants, 30r, 30f and 30D3, contained trace, reduced and almost-normal amounts of
, respectively (Fig. 2a
). We showed that this was due to different expression levels of cpcC1. This gene undergoes a polar effect from the Km cassette inserted upstream in 30f and 30r and from the downstream
cassette insertion in
30D3. These polar effects resulted in a decreased amount of the cpcC1 product,
; consequently the amount of PC incorporated in the PBS decreased. This result suggests that transcriptional regulation of the rod-linker genes could adjust the light-harvesting capacity of the PBS by modulating the amounts of PC incorporated into the rods. Decrease of the level of a larger transcript relative to a smaller one in response to high light levels has been shown to occur in the cpc operon of Anabaena PCC7120 (Belknap & Haselkorn, 1987
). The relative level of the transcripts could be modulated through transcription termination at the stemloop downstream of cpcA or by RNA processing at this site followed by degradation of the linker-encoding mRNA. In Synechocystis sp. strain PCC6803 and Synechococcus sp. strain PCC6301 PBSs, the
to
ratio was repeatedly <1, decreasing under high-light conditions (our unpublished observations; Lönneborg et al., 1985
). In view of the cpcC2 and cpcC1 co-transcription, one must imagine a form of regulation in which cpcC2 is down-regulated first. Endoribonuclease processing downstream of cpcA followed by 5'
3' progressing degradation (Rauhut & Klug, 1999
) of the linker-encoding RNA could accomplish this, since cpcC2 would be down-regulated first and cpcC1 would be protected by the 3' stemloop structures. Further experiments are needed to test this hypothesis.
The CB mutant is similar to the An112 mutant of Synechococcus sp. strain PCC6301 (Yamanaka et al., 1980) and the PR6009 mutant of Synechococcus sp. strain PCC7002 (de Lorimier et al., 1990b
). All these mutants show that LRC is involved in association of the core-proximal PC hexamers, at the base of every rod, with the core. Two modes of assembly are then possible for the remaining PC hexamers: (i)
and
are interchangeable either can be present in both the intermediary and distal PC hexamers; (ii) the intermediary PC hexamers contain only one linker type, with the other specifically present in the distal PC hexamers. Careful characterization of mutants deficient in each of these linkers should favour one of these modes. Such mutants constructed in Synechococcus sp. strain PCC7942 suggested that
could replace
in its absence (Bhalerao et al., 1991
, 1993
), favouring the first mode but in contradiction with the results presented here. Indeed, the first mode was excluded by two of our observations: (i) the absence of
prevented
attachment in the cpcC1-deficient strain 33, and (ii) transcomplementation of strain 33 with cpcC1 restored attachment of both
and
. We therefore favour the second mode, with
attaching the intermediary PC hexamer and
attaching the distal one. This mode is also in agreement with results obtained upon nitrogen starvation, where sequential loss of PC and associated linkers occurs.
disappears first from the PBS of Synechocystis sp. strain PCC6803 and Synechococcus sp. strain PCC6301 during the initial steps of nitrogen starvation, suggesting that this linker is associated with the peripheral PC hexamer (Richaud et al., 2001
; Yamanaka & Glazer, 1980
). In terms of genetics, cpcC2 and cpcC1 might have been created by gene duplication in an ancestral strain that contained only one cpcC, such as Synechococcus sp. strain PCC7002. The resulting genes then acquired different functions, and cpcC1 became epistatic to cpcC2. The domain that determines the specificity of
and
may lie within the C-terminal third of their sequences, since it is less conserved than the remaining two-thirds (28 % and 55 % identity for each, respectively). Specific interactions between these rod linkers seem to exclude their random insertion in Synechocystis sp. strain PCC6803 but not in mutants of Synechococcus sp. strain PCC7942. Amino acid sequence comparison of
and
from Synechocystis sp. strain PCC6803 and Synechococcus sp. strain PCC7942 did not provide an explanation for the differing results obtained in the two strains.
was present, albeit in smaller amounts, in PBSs lacking the core-distal (30f) or both the intermediary and the core-distal PC hexamers (33 and CB). Its reduced level was first attributed to the polar effect of the Km cassette on cpcD expression in these strains, but the increased amounts of
in the 33c PBS compared to CBc (Fig. 4a
) suggests that, although the polar effect exists,
might have a higher affinity for a PC hexamer containing
. Indeed
was proposed to be associated with the distal end of the rods (de Lorimier et al., 1990a
). Its absence does not seem to affect PBS assembly or function in Synechocystis sp. strain PCC6803.
In cyanobacteria, the FNR contains an N-terminal domain that shares similarity to PBS linker polypeptides (Schluchter & Bryant, 1992). The highest similarity was found to the
linker (about 32 % identity and 75 % similarity over 80 amino acids), while lower similarities were found to the C-terminal domains of
and
, and even to the core-associated linker LC. It has been proposed that the FNR shares the same binding site as
in the PBS rod of Synechococcus sp. strain PCC7002 (Gomez-Lojero et al., 2003
). If they shared the same binding site, one would expect the relative amounts of FNR to increase in the absence of
, which was not observed in any of the mutants constructed here. The binding site of the FNR has also been suggested to be the core-proximal PC hexamer in Synechocystis sp. strain PCC6803 (van Thor et al., 1999
), but more direct evidence is needed in order to localize the linkers and the FNR in the PBS.
![]() |
ACKNOWLEDGEMENTS |
---|
![]() |
REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Ajlani, G. & Vernotte, C. (1998). Construction and characterization of a phycobiliprotein-less mutant of Synechocystis sp. PCC 6803. Plant Mol Biol 37, 577580.[CrossRef][Medline]
Ajlani, G., Vernotte, C., DiMagno, L. & Haselkorn, R. (1995). Phycobilisome core mutants of Synechocystis PCC 6803. Biochim Biophys Acta 1231, 189196.
Allen, M. M. (1968). Simple conditions for growth of unicellular blue-green algae on plates. J Phycol 4, 14.
Allen, M. M. & Smith, A. J. (1969). Nitrogen chlorosis in blue-green algae. Arch Mikrobiol 69, 114120.[CrossRef][Medline]
Belknap, W. R. & Haselkorn, R. (1987). Cloning and light regulation of expression of the phycocyanin operon of the cyanobacterium Anabaena. EMBO J 6, 871884.[Abstract]
Bhalerao, R. P. & Gustafsson, P. (1994). Factors influencing the phycobilisome rod composition of the cyanobacterium Synechococcus sp. PCC7942: effects of reduced phycocyanin content, lack of rod-linkers and over-expression of the rod-terminating linker. Physiol Plant 90, 187197.[CrossRef]
Bhalerao, R. P., Gillbro, T. & Gustafsson, P. (1991). Structure and energy transfer of the phycobilisome in a linker protein replacement mutant of cyanobacterium Synechococcus 7942. Biochim Biophys Acta 1060, 5966.
Bhalerao, R. P., Lind, L. K., Persson, C. E. & Gustafsson, P. (1993). Cloning of the phycobilisome rod linker genes from the cyanobacterium Synechococcus sp. PCC 6301 and their inactivation in Synechococcus sp. PCC 7942. Mol Gen Genet 237, 8996.[CrossRef][Medline]
Bruce, D., Brimble, S. & Bryant, D. A. (1989). State transitions in a phycobilisome-less mutant of the cyanobacterium Synechococcus sp. PCC 7002. Biochim Biophys Acta 974, 6673.[Medline]
Cai, Y. & Wolk, C. P. (1990). Use of a conditionally lethal gene in Anabaena sp. strain PCC 7120 to select for double recombinants and to entrap insertion sequences. J Bacteriol 172, 31383145.[Medline]
Collier, J. L. & Grossman, A. R. (1994). A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. EMBO J 13, 10391047.[Abstract]
de Lorimier, R., Bryant, D. A. & Stevens, S. E., Jr (1990a). Genetic analysis of a 9 kDa phycocyanin-associated linker polypeptide. Biochim Biophys Acta 1019, 2941.[Medline]
de Lorimier, R., Guglielmi, G., Bryant, D. A. & Stevens, S. E., Jr (1990b). Structure and mutation of a gene encoding a Mr 33,000 phycocyanin-associated linker polypeptide. Arch Microbiol 153, 541549.[CrossRef][Medline]
de Marsac, N. T. & Cohen-Bazire, G. (1977). Molecular composition of cyanobacterial phycobilisomes. Proc Natl Acad Sci U S A 74, 16351639.[Abstract]
Elmorjani, K., Thomas, J.-C. & Sebban, P. (1986). Phycobilisomes of wild type and pigment mutants of the cyanobacterium Synechocystis PCC 6803. Arch Microbiol 146, 186191.
Fling, S. P. & Gregerson, D. S. (1986). Peptide and protein molecular weight determination by electrophoresis using a high-molarity tris buffer system without urea. Anal Biochem 155, 8388.[Medline]
Garnier, F., Dubacq, J. P. & Thomas, J. C. (1994). Evidence for a transient association of new proteins with the Spirulina maxima phycobilisome in relation to light Intensity. Plant Physiol 106, 747754.
Glazer, A. N. (1988). Phycobilisomes. Methods Enzymol 167, 304312.
Glazer, A. N. (1989). Light guides. Directional energy transfer in a photosynthetic antenna. J Biol Chem 264, 14.
Golden, J. W. & Wiest, D. R. (1988). Genome rearrangement and nitrogen fixation in Anabaena blocked by inactivation of xisA gene. Science 242, 14211423.[Medline]
Gomez-Lojero, C., Perez-Gomez, B., Shen, G., Schluchter, W. M. & Bryant, D. A. (2003). Interaction of ferredoxin : NADP+ oxidoreductase with phycobilisomes and phycobilisome substructures of the cyanobacterium Synechococcus sp. strain PCC 7002. Biochemistry 42, 1380013811.[CrossRef][Medline]
Imashimizu, M., Fujiwara, S., Tanigawa, R., Tanaka, K., Hirokawa, T., Nakajima, Y., Higo, J. & Tsuzuki, M. (2003). Thymine at 5 is crucial for cpc promoter activity of Synechocystis sp. strain PCC 6714. J Bacteriol 185, 64776480.
Lagarde, D., Beuf, L. & Vermaas, W. (2000). Increased production of zeaxanthin and other pigments by application of genetic engineering techniques to Synechocystis sp. strain PCC 6803. Appl Environ Microbiol 66, 6472.
Lönneborg, A., Lind, L. K., Kalla, S. R., Gustafsson, P. & Öquist, G. (1985). Acclimation processes in the light-harvesting system of the cyanobacterium Anacystis nidulans following a light shift from white to red light. Plant Physiol 78, 110114.
Luque, I., Ochoa De Alda, J. A., Richaud, C., Zabulon, G., Thomas, J. C. & Houmard, J. (2003). The NblAI protein from the filamentous cyanobacterium Tolypothrix PCC 7601: regulation of its expression and interactions with phycobilisome components. Mol Microbiol 50, 10431054.[CrossRef][Medline]
Mohamed, A. & Jansson, C. (1989). Influence of light on accumulation of photosynthesis-specific transcripts in the cyanobacterium Synechocystis 6803. Plant Mol Biol 13, 693700.[Medline]
Oka, A., Sugisaki, H. & Takanami, M. (1981). Nucleotide sequence of the kanamycin resistance transposon Tn903. J Mol Biol 147, 217226.[Medline]
Prentki, P. & Krisch, H. M. (1984). In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29, 303313.[CrossRef][Medline]
Rauhut, R. & Klug, G. (1999). mRNA degradation in bacteria. FEMS Microbiol Rev 23, 353370.[CrossRef][Medline]
Richaud, C., Zabulon, G., Joder, A. & Thomas, J. C. (2001). Nitrogen or sulfur starvation differentially affects phycobilisome degradation and expression of the nblA gene in Synechocystis strain PCC 6803. J Bacteriol 183, 29892994.
Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
Schluchter, W. M. & Bryant, D. A. (1992). Molecular characterization of ferredoxin-NADP+ oxidoreductase in cyanobacteria: cloning and sequence of the petH gene of Synechococcus sp. PCC 7002 and studies on the gene product. Biochemistry 31, 30923102.[Medline]
Sidler, W. A. (1994). Phycobilisome and phycobiliprotein structures. In The Molecular Biology of Cyanobacteria, pp. 139216. Edited by D. A. Bryant. Dordrecht: Kluwer.
van Thor, J. J., Gruters, O. W., Matthijs, H. C. & Hellingwerf, K. J. (1999). Localization and function of ferredoxin : NADP(+) reductase bound to the phycobilisomes of Synechocystis. EMBO J 18, 41284136.
Vioque, A. (1992). Analysis of the gene encoding the RNA subunit of ribonuclease P from cyanobacteria. Nucleic Acids Res 20, 63316337.[Abstract]
Yamanaka, G. & Glazer, A. N. (1980). Dynamic aspects of phycobilisome structure. Arch Microbiol 124, 3947.
Yamanaka, G., Glazer, A. N. & Williams, R. C. (1980). Molecular architecture of a light-harvesting antenna. Comparison of wild type and mutant Synechococcus 6301 phycobilisomes. J Biol Chem 255, 1110411110.[Medline]
Received 20 July 2004;
revised 20 September 2004;
accepted 20 September 2004.
HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
INT J SYST EVOL MICROBIOL | MICROBIOLOGY | J GEN VIROL |
J MED MICROBIOL | ALL SGM JOURNALS |