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First published online July 30, 2008; 10.1104/pp.108.123505 Plant Physiology 148:660-670 (2008) © 2008 American Society of Plant Biologists An AbrB-Like Transcriptional Regulator, Sll0822, Is Essential for the Activation of Nitrogen-Regulated Genes in Synechocystis sp. PCC 68031,[W]Department of Biochemistry and Molecular Biology, Graduate School of Science and Engineering, Saitama University, Sakura-ku, Saitama 338–8570, Japan
Every cyanobacterial species possesses multiple genes encoding AbrB-like transcriptional regulators (cyAbrBs) distinct from those conserved among other bacterial species. In this study, two genes encoding cyAbrBs in Synechocystis sp. PCC 6803, sll0359 and sll0822, were insertionally disrupted in order to examine their physiological roles. A fully segregated disrupted mutant of sll0822 (  sll0822 mutant) but not of sll0359 was obtained, although both mutants exhibited similar phenotypes (i.e. decreases in growth rate and pigment content). The growth rate of the sll0822 mutant was low under any condition, but the low pigment content could be partially recovered by nitrate supplementation of the medium. DNA microarray and RNA-blot analyses revealed that the level of expression of a part of the NtcA regulon, such as urtA, amt1, glnB, sigE, and the nrt operon, was significantly decreased in the sll0822 mutant, although the induction of these genes upon nitrogen depletion was still observed to some extent. Sll0822 seems to work in parallel with NtcA to achieve flexible regulation of the nitrogen uptake system. The Sll0822 protein exists mainly in a dimeric form in vivo, and the amount of the protein was not affected by nitrogen availability. This observation, together with the low binding specificity of the purified histidine-tagged Sll0822 protein, implies that the activity of Sll0822 may be posttranslationally modulated in Synechocystis cells.
Following changes in environmental conditions such as photon flux density, temperature, or nutrient availability, photosynthetic organisms must modulate photosynthetic activity and various metabolic processes in order to acclimate to the new environment. The acclimation responses of the cyanobacterium Synechocystis sp. PCC 6803 are well characterized with regard to transcriptional regulation. Genome-wide investigations of gene expression using DNA microarray techniques have allowed the identification of a set of genes induced or repressed upon environmental change (Los et al., 2007  ). In order to understand the signal transduction mechanisms responsible for the changes in the gene expression profile, identification of transcriptional regulators working in response to environmental changes is essential. We have been characterizing putative transcriptional regulators that are highly conserved in cyanobacterial genomes but not in other bacterial genomes, since such regulators must play an important role in photosynthetic organisms. For example, PedR, a small LuxR-type regulator specific to cyanobacterial species, was shown to regulate gene expression, depending on the availability of reducing equivalents supplied from the photosynthetic electron transport chain (Nakamura and Hihara, 2006).
In this study, we focused on AbrB-like transcriptional regulators in cyanobacteria. Genes encoding AbrB-like transcriptional regulators have been discovered in a wide variety of gram-positive, gram-negative, and archaeal species (Vaughn et al., 2000
Cyanobacterial AbrB proteins (hereafter called cyAbrBs) are unique in that they have an AbrB-like DNA-binding domain in the C terminal region. Multiple copies of genes encoding cyAbrBs are found in every cyanobacterial genomic sequence now available, whereas AbrB-like regulators having DNA-binding domains at their C termini are not conserved in other bacterial species. Very recently, Oliveira and Lindblad (2008) Here, we report that Sll0822, one of the cyAbrBs in Synechocystis sp. PCC 6803, plays an important role in the activation of nitrogen-regulated genes. The low growth rate and pigment content of the gene-disrupted mutant revealed the physiological significance of transcriptional regulation by Sll0822.
Phylogenetic Analysis of cyAbrBs Multiple genes encode cyAbrBs in every cyanobacterial genome. Among 32 cyanobacterial species whose genomic sequences are available (January 2008), 23 species have two copies, and six species possess three copies, of genes encoding cyAbrB. Synechococcus sp. CC 9902 and Synechococcus sp. CC 9605 have four and five copies, respectively. It is notable that there are 14 copies on the chromosome and plasmids of Acaryochloris marina. Figure 1 shows the phylogenetic tree of cyAbrBs from 12 representative species. In most cases, multiple copies in a single organism are classified into two different clades, clades A and B. The marine unicellular non-N2-fixing species also have a set of cyAbrBs categorized into two different clades, marine clades A and B. These marine regulators are distinct from other cyAbrBs in that their N-terminal end is about 10 amino acids shorter (Supplemental Fig. S1). In the case of A. marina, two copies are classified into clades A and B and the remaining 12 copies form a distinct clade. CyAbrBs of Gloeobacter violaceus PCC 7421 and Synechococcus elongatus PCC 7942 do not belong to any of the groups mentioned above.
Supplemental Figure S1 shows a comparison of the amino acid sequences of cyAbrBs used for the generation of the phylogenetic tree. The N-terminal regions of cyAbrBs are highly conserved but show no significant homology to known protein motifs. In the C-terminal region, the overall structure of the ββ  ββ motif characteristic of AbrB-like DNA-binding domains (Coles et al., 2005) is well conserved among cyAbrBs, although sequence similarity to AbrB itself is rather low. The sequence identity of cyAbrBs between clades A and B is approximately 50%.
Synechocystis sp. PCC 6803 possesses two genes for cyAbrB, sll0359 (clade A) and sll0822 (clade B), as well as three genes for the AbrB-like regulators, slr0724, ssl1300, and ssr7040, which have N-terminal DNA-binding domains. To elucidate the function of the cyAbrBs and the physiological significance of a set of cyAbrBs belonging to two different clades, we individually inactivated both sll0359 and sll0822 by insertion of an antibiotic resistance cassette (Supplemental Fig. S2A). The
Figure 2 shows the growth properties and pigment contents of wild-type and sll0822 mutant cells under different photon flux densities. The upshift of photon flux density did not improve the growth of the mutant. The growth of the sll0822 mutant was always slower than that of the wild type under a given light condition (Fig. 2A
). The pigment content of the mutant decreased normally upon the upshift of photon flux density (Fig. 2, B and C), indicating that the capacity for light acclimation was not abolished by inactivation of sll0822.
Nitrogen availability significantly affects cellular pigment content in cyanobacterial cells (Allen and Smith, 1969 ; Collier and Grossman, 1992). Thus, we examined the effect of nitrogen availability on the growth properties and pigment content of the sll0822 mutant. When cells were transferred from normal BG11 medium to nitrogen-free medium, growth inhibition (Fig. 3A
) and a decrease in pigment content (Fig. 3, B and C) were similar in both the wild type and the sll0822 mutant. Supplementation of normal BG11 medium with a 4-fold excess of nitrate (final concentration = 70.6 mM) did not affect the growth properties of either strain (Fig. 3A). However, the pigment content of the mutant, especially phycocyanin content, was significantly recovered by supplementation with nitrate (Fig. 3, B and C).
Identification of Target Genes of Sll0822
To identify the target genes of Sll0822, we performed DNA microarray analysis of wild-type and
Next, we investigated whether Sll0822 can bind to the upstream regions of the above listed putative target genes. Recombinant His-tagged Sll0822 was overexpressed in Escherichia coli, purified to near homogeneity (Supplemental Fig. S3), and used for gel mobility shift assays with upstream DNA fragments of putative target genes. The binding specificity of the His-Sll0822 protein appeared to be low, since nonspecific band shifts with unrelated DNA sequences were observed upon the addition of 40 ng of His-Sll0822 protein (data not shown). However, when 20 ng of His-Sll0822 protein was added, the interaction with the specific promoters was reproducibly observed (Fig. 4 ). His-Sll0822 bound to the upstream regions of nrtABCD and amt1, whose expression levels were lowered by disruption of sll0822. On the other hand, no band shifts were observed using the upstream regions of psaFJ and psaK1, although expression of these genes was also lowered in the sll0822 mutant. As for urtA, glnB, and sigE, a slightly shifted smear was observed upon the addition of 20 ng of His-Sll0822 (data not shown). The upstream regions of sll0330, slr1704, and groESL, whose expression levels were increased in the sll0822 mutant, did not show an interaction with His-Sll0822.
Many AbrB-like regulators having N-terminal DNA-binding domains are negatively autoregulated (Strauch et al., 1989 ; Bagyan et al., 1996). Thus, we tested the binding of His-Sll0822 to its own promoter region (Fig. 4). Mobility of the sll0822 upstream DNA fragment was clearly altered by incubation with purified His-Sll0822. On the other hand, no band shift was observed with the upstream region of sll0359.
In cyanobacteria, most of the genes encoding nitrogen assimilation enzymes or transporters are repressed by ammonium, and their transcription is activated by the transcriptional factor NtcA in the absence of ammonium (Herrero et al., 2001
To examine the amount and oligomerization state of the Sll0822 protein in vivo, crude extracts of wild-type cells under different nitrogen conditions were subjected to immunoblot analysis using polyclonal antibodies raised against purified Sll0822. No band was detected when a crude extract from the sll0822 mutant was used, demonstrating that the Sll0822 antibody did not cross-react with the Sll0359 protein (data not shown). When a crude extract of wild-type cells was separated by SDS-PAGE, Sll0822 protein was detected mainly as a monomer of 17 kD (data not shown). To detect the native oligomerization state of Sll0822, we treated the crude extract with the cross-linker 1-ethyl-3-(3-dimethylaminopropyl)-carbodiimide (EDC) prior to separation by SDS-PAGE. Most of the Sll0822 protein was detected as a dimeric form of 34 kD by this method (Fig. 6
). This observation suggests that the oligomeric structure of cyAbrB is different from that of AbrB in B. subtilis, since AbrB was shown to exist as a tetramer in vivo. We observed that the banding pattern of Sll0822 remained unchanged after both 1 h (data not shown) and 12 h (Fig. 6) of incubation under different nitrogen conditions. It is of note that neither the amount nor the oligomerization state of Sll0822 was affected by the different nitrogen conditions.
Physiological Significance of Sll0822
In this study, we identified Sll0822 as a novel regulator essential for the high-level expression of nitrogen-controlled genes. Upon disruption of the sll0822 gene, the expression levels of several members of the NtcA regulon, such as the nrt operon, urtA-E, amt1-3, glnB, and sigE, decreased significantly irrespective of nitrogen conditions, although the induction upon nitrogen depletion was still observed to some extent (Fig. 5). The nrt, urt, and amt genes encode components of the nitrate/nitrite transporter, urea transporter, and ammonium permease, respectively. It is likely that Sll0822 is important for the normal expression of nitrogen uptake systems. The growth rates and pigment contents of
The partial overlap of the target genes of Sll0822 with those of NtcA raises a question concerning the relationship between these two regulators. Sll0822 is not located upstream of NtcA in the signal transduction cascade, considering that transcript levels of ntcA were not affected by the disruption of sll0822 (Fig. 5). Similarly, it is not likely that NtcA regulates the transcript level of sll0822, since no NtcA-binding site was found in the upstream region of sll0822. As for the possibility of protein-protein interactions, neither the cross-linking experiment conducted in this study (Fig. 6) nor a yeast two-hybrid assay performed at the Kazusa DNA Research Institute (Sato et al., 2007
To date, several studies have identified additional factors required for the transcriptional regulation of NtcA-regulated genes in Synechocystis sp. PCC 6803. For example, the nrtA operon and the nirA operon involved in nitrate assimilation require the LysR family regulator NtcB for high-level expression and for nitrite-responsive activation (Aichi et al., 2001
Transcript levels of sll0822 decreased under nitrogen-depleted conditions (Fig. 5), which may be a result of negative autoregulation. After 12 h of incubation, the sll0822 transcript was barely detectable, whereas the amount of Sll0822 protein remained unchanged (Fig. 6). This indicates that Sll0822 is a highly stable protein, and transcriptional regulation may not be important for the regulation of its activity. Instead, it is possible that the regulation of Sll0822 is achieved by posttranslational modification, as inferred from the information described below. Two-dimensional gel electrophoresis of the soluble fraction of Synechocystis sp. PCC 6803 (Sazuka et al., 1999
At least two genes encoding cyAbrBs are found in every cyanobacterial genome currently available. A set of genes belonging to clades A and B is conserved in most cases (Fig. 1), and this corresponds to sll0359 and sll0822 in Synechocystis sp. PCC 6803. Disruption of either sll0359 or sll0822 resulted in decreases in growth rate and pigment content (Table I). This indicates that cyAbrBs belonging to both clades A and B are required for normal cell growth and that their function is not redundant. Sll0359 may play a more important role than Sll0822, considering that complete segregation was attained in the
This study revealed the importance of Sll0822, one of two cyAbrBs in Synechocystis sp. PCC 6803, in the activation of nitrogen-regulated genes. In the sll0822 mutant, significant decreases in growth rate and cellular pigment content were observed, demonstrating the physiological significance of this protein. Sll0822 existed mainly in a dimeric form in vivo, and its amount was not affected by nitrogen availability. The other cyAbrB in Synechocystis sp. PCC 6803, Sll0359, was shown to be essential for growth, and a decrease in copy number of sll0359 resulted in a phenotype similar to that observed in the sll0822 mutant. Significant conservation of multiple genes encoding cyAbrBs among cyanobacterial genomes implies that these multiple genes have their own specific roles in regulatory processes. Additional studies on the interactions between Sll0822 and Sll0359 should further unravel the mechanisms of transcriptional regulation.
Strains and Culture Conditions
A Glc-tolerant wild-type strain of Synechocystis sp. PCC 6803 was grown at 32°C in BG11 medium containing 20 mM HEPES-NaOH, pH 7.0, under continuous illumination at 20 µmol photons m–2 s–1 with bubbling of air. Mutants were grown under the same conditions, except that antibiotics were added to the medium: 20 µg mL–1 kanamycin for
A gene-flanking segment of sll0822 (900 bp; nucleotides 2,862,739–2,861,840 according to the numbering in CyanoBase) was amplified by PCR from genomic DNA of the wild-type strain using the primers 0822delF (5'-CGTCGCAGGGTAATCAAC-3') and 0822delR (5'-GTATGAGGAAATCAACAG-3') and cloned into the pT7Blue T-vector (Novagen). A kanamycin resistance cartridge, which had been excised from the plasmid pRL161 by digestion with HincII, was inserted into the coding region of sll0822 at the StyI site. For the construction of the
In vivo absorption spectra of whole cells suspended in BG11 medium were measured at room temperature using a spectrophotometer (model 557; Hitachi) with an end-on photomultiplier. Chlorophyll content was calculated from the peak heights of absorption spectra using the equations of Arnon et al. (1974)
Isolation of total RNA using the RNeasy Midi kit (Qiagen) and subsequent DNA microarray analysis with CyanoCHIP (version 1.6; Takara) were performed as described previously (Hihara et al., 2003
The sll0822 coding region was PCR amplified using the primers 0822-F (5'-AACATATGGCTAAATCAAACGCA-3') and 0822-R (5'-AAGGATCCTTACTCTTCTTCGTCGTC-3'), cloned into the pT7Blue T-vector (Novagen), digested with NdeI and BamHI (sites underlined), and subcloned into the same restriction sites in pET28a (Novagen) to create pET0822 for the expression of a fusion protein with an N-terminal His tag. The nucleotide sequence was confirmed by DNA sequencing using the BigDye terminator method (Applied Biosystems). Escherichia coli BL21(DE3) harboring pET0822 was grown to an OD600 of 0.6 in 500 mL of 2x yeast extract-tryptone medium containing 20 µg mL–1 kanamycin, induced with 0.013% isopropyl β-D-thiogalactoside for 5 h, and harvested by centrifugation. Cells were resuspended in 15 mL of 20 mM phosphate buffer, pH 7.4, containing 0.5 M NaCl and 60 mM imidazole and disrupted by 10 rounds of sonication for 30 s each at 4°C. After the removal of whole cells and insoluble material by centrifugation, the soluble protein fraction was filtered through a 0.2-µm filter (DISMIC-25cs; ADVANTEC). His-Sll0822 was purified by nickel-affinity column chromatography using a HiTrap Chelating HP column (Amersham Biosciences). The soluble protein fraction was applied to the column equilibrated with 20 mM phosphate buffer, pH 7.4, containing 0.5 M NaCl and 60 mM imidazole, washed with the same buffer, and eluted with 20 mM phosphate buffer, pH 7.4, containing 0.5 M NaCl and 300 mM imidazole. Purified His-Sll0822 was desalted by a HiTrap Desalting column (Amersham Biosciences). Protein composition was examined by electrophoresis on a 15% (w/v) SDS-polyacrylamide gel followed by staining with Coomassie Brilliant Blue R-250.
For preparation of the probes for gel mobility shift assays, the following DNA fragments corresponding to the whole intergenic region upstream of each gene were obtained by PCR amplification: sll0822 (nucleotides 2,862,557–2,862,395 according to the numbering in CyanoBase; 163 bp), nrtABCD (1,010,709–1,010,575; 135 bp), psaFJ (1,688,212–1,688,054; 135 bp), psaK1 (156,259–156,390; 132 bp), sll0359 (2,146,387–2,146,586; 200 bp), slr1704 (728,490–728,659; 170 bp), and groESL (915,053–915,312; 260 bp). In the case of the following genes with long intergenic regions, a part of the intergenic region was amplified: amt1 (2,971,201–2,971,400; 200 bp) and sll0330 (2,385,028–2,384,729; 300 bp). The 3' end of the DNA fragment for each probe was labeled with digoxigenin (DIG)-ddUTP by the terminal transferase method according to the manufacturer's instructions (DIG Gel Shift kit; Roche). Assays were performed using a DIG Gel Shift kit as described previously (Nakamura and Hihara, 2006
Isolation of RNA by the hot phenol method and RNA-blot analyses, using a DIG RNA Labeling and Detection kit (Roche), were performed as described previously (Muramatsu and Hihara, 2003
Fifty milliliters of exponential growth phase cell culture was harvested by centrifugation. The pellet was resuspended in 200 µL of breakage buffer (20 mM Tris-HCl, pH 8.0, and 100 mM NaCl). The cell suspension was mixed with approximately 100 µL of glass beads (diameter, 0.1 mm; BioSpec Products), and cells were disrupted by four rounds of vigorous vortexing for 2 min followed by cooling on ice for 1 min. After removal of unbroken cells and debris by centrifugation at 700g for 3 min, cell extracts were mixed with an equal volume of 2x SDS sample buffer (62.5 mM Tris-HCl, pH 6.8, 4% SDS [w/v], 20% glycerol [v/v], and 0.01% bromphenol blue [w/v]). SDS-gel electrophoresis was performed according to the procedure of Laemmli (1970)
The following materials are available in the online version of this article.
Received May 25, 2008; accepted July 23, 2008; published July 30, 2008.
1 This work was supported by a Grant-in-Aid for Young Scientists from the Japan Society for the Promotion of Science (to Y.H.).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Yukako Hihara (hihara{at}molbiol.saitama-u.ac.jp).
[W] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.108.123505 * Corresponding author; e-mail hihara{at}molbiol.saitama-u.ac.jp.
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