Logo of pnasPNASInfo for AuthorsSubscriptionsAboutThis Article
Proc Natl Acad Sci U S A. 1999 Nov 9; 96(23): 13571–13576.
Plant Biology

Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC 7942


Exposure of cells of cyanobacteria (blue–green algae) grown under high-CO2 conditions to inorganic C-limitation induces transcription of particular genes and expression of high-affinity CO2 and HCO3 transport systems. Among the low-CO2-inducible transcription units of Synechococcus sp. strain PCC 7942 is the cmpABCD operon, encoding an ATP-binding cassette transporter similar to the nitrate/nitrite transporter of the same cyanobacterium. A nitrogen-regulated promoter was used to selectively induce expression of the cmpABCD genes by growth of transgenic cells on nitrate under high CO2 conditions. Measurements of the initial rate of HCO3 uptake after onset of light, and of the steady-state rate of HCO3 uptake in the light, showed that the controlled induction of the cmp genes resulted in selective expression of high-affinity HCO3 transport activity. The forced expression of cmpABCD did not significantly increase the CO2 uptake capabilities of the cells. These findings demonstrated that the cmpABCD genes encode a high-affinity HCO3 transporter. A deletion mutant of cmpAB (M42) retained low CO2-inducible activity of HCO3 transport, indicating the occurrence of HCO3 transporter(s) distinct from the one encoded by cmpABCD. HCO3 uptake by low-CO2-induced M42 cells showed lower affinity for external HCO3 than for wild-type cells under the same conditions, showing that the HCO3 transporter encoded by cmpABCD has the highest affinity for HCO3 among the HCO3 transporters present in the cyanobacterium. This appears to be the first unambiguous identification and description of a primary active HCO3 transporter.

Cyanobacteria possess a CO2-concentrating mechanism (CCM), which elevates the CO2 concentration around the active site of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and thereby enables efficient CO2 fixation despite the low affinity and selectivity of their Rubisco for CO2 (1, 2). The CCM involves the abilities to actively transport inorganic C (CO2 and HCO3; designated Ci) into the cell, to accumulate Ci as HCO3 in the cytoplasm, and to effectively convert HCO3 into CO2 in carboxysomes, the polyhedral inclusion bodies to which Rubisco is localized. The Ci-transporting mechanism plays a major role in adaptation of cyanobacteria to changing availability of Ci. Cells grown under high-CO2 conditions (1–5% CO2, vol/vol) have low-affinity Ci transport activities and incubation of the cells under low-CO2 conditions (0.035% CO2 or less, vol/vol) induces expression of high-affinity Ci transport activities. Physiological studies have suggested the occurrence of multiple forms of Ci transporters, which are distinct in substrate specificity (HCO3 or CO2), affinity for the substrate, inducibility by Ci limitation, and requirement for Na+ (1, 2). The genes for Ci transporters have been sought after for some time, partly because of their potential for improving the nitrogen and water-use efficiency of photosynthesis when introduced into higher plants performing C3-type photosynthesis.

Genetic analysis of cyanobacterial mutants that require high-CO2 concentrations for growth has identified >10 genes directly related to the CCM, but most of them are involved in assembly and functioning of the carboxysome (2). The Synechocystis sp. strain PCC 6803 mutants with impaired Ci transport activities are defective either in the ndh genes [encoding the subunits of NAD(P)H dehydrogenase] that are presumably involved in energization of Ci transporters (3), or in the pxcA (cotA) gene, which is required for H+ extrusion into the external medium and is indirectly involved in CO2 transport (4). Analysis of high-CO2-requiring mutants of Synechococcus sp. strain PCC 7942, on the other hand, identified a gene (ictB) necessary for HCO3 transport (5). Targeted inactivation of this gene results in loss of HCO3-transporting activity in cells grown under high-CO2 conditions and practically abolishes induction of high-affinity HCO3 transport activity under low-CO2 conditions (5). However, ictB is unlikely to encode a HCO3 transporter, because the profound effect of the ictB mutation on HCO3-transporting activity is incompatible with the presumed occurrence of multiple HCO3 transporters. Thus, no mutants defective in Ci transporters have been identified to date.

Studies on the membrane proteins of Synechococcus sp. strain PCC 7942, on the other hand, identified a 42-kDa plasma membrane protein synthesized under C-limited conditions (6). The coinduction of the protein, concomitantly with enhanced Ci-transport activity, suggested that the protein may play a role in Ci transport (6, 7), but at the time, this possibility was considered unlikely because the protein deduced from the nucleotide sequence of the gene (cmpA) was largely hydrophilic and a deletion mutant (M42) of the gene showed low-CO2-inducible activities of CO2 and HCO3 transport (8). Later studies showed that cmpA forms a gene cluster with three genes located downstream (cmpB, cmpC, and cmpD) that encode a set of proteins comprising a membrane complex of an ATP-binding cassette (ABC) transporter (ref. 9, GenBank accession no. D26358). The genes nrtA, nrtB, nrtC, and nrtD, which are strongly similar to cmpA, cmpB, cmpC, and cmpD, respectively, were shown to encode a nitrate/nitrite bispecific transporter (10, 11), with the nrtA gene product acting as the membrane-anchored substrate-binding protein (12). Thus, the 42-kDa protein is likely to be the substrate-binding protein of a transporter encoded by cmpABCD. The presumed occurrence of multiple Ci transporters would account for the presence of inducible Ci transport activities in M42. On the basis of these considerations, we have reinvestigated the role of the cmp genes. The genes are shown to constitute a low-CO2-inducible operon. By selective induction of the cmp genes under high-CO2 conditions, by using a nitrogen-regulated promoter of the nirA operon (13), it is shown that cmpABCD encodes a high-affinity HCO3 transport system.

Materials and Methods

Strains and Growth Conditions.

Cells of the wild-type (WT) Synechococcus sp. strain PCC 7942, mutant M42 (8), and a genetically engineered mutant derived herein (see below) were grown photoautotrophically at 30°C under continuous illumination provided by fluorescent lamps. The basal medium used was a nitrogen-free medium obtained by modification of BG11 medium (14) as described previously (15). Nitrate-containing medium and ammonium-containing medium were prepared by addition of 15 mM KNO3 or 3.75 mM (NH4)2SO4, respectively, to the basal medium. The media were buffered with either 20 mM Hepes-KOH (pH 8.0) or 10 mM 1,3-bis[tris(hydroxymethyl)methylamino]propane (BTP)-HCl (pH 8.0). When appropriate, kanamycin and spectinomycin were added to the media at 15 and 10 μg/ml, respectively.

The cultures were routinely maintained under high-CO2 conditions, i.e., aeration with 2% (vol/vol) CO2 in air, under illumination at 90 μmol of photons m−2[center dot]s−1. For the experiments involving induction of Ci transport activities in the CMP+ mutant under high-CO2 conditions, cultures were grown at a light intensity of 250 μmol of photons m−2[center dot]s−1. For the other experiments, involving induction of Ci transport activities by Ci limitation, cells were grown under a light intensity of 90 μmol of photons m−2[center dot]s−1 so as to minimize photoinhibitory damage to the cells, which becomes prominent at high light intensities and low CO2 concentrations (16, 17). For transfer of ammonium-grown cells to nitrate-containing medium under the high-CO2 conditions, cells grown to the mid-logarithmic phase of growth were collected by centrifugation at 5,000 × g for 5 min at 25°C, washed twice with the nitrogen-free medium by resuspension and recentrifugation, inoculated into nitrate-containing medium, and incubated under the same general conditions as before. For transfer of high-CO2-grown cells to low-CO2 conditions, cells were grown in nitrate-containing medium, collected by centrifugation as described above, washed twice with the growth medium by resuspension and recentrifugation, inoculated into fresh nitrate-containing medium, and aerated with air containing 0.002–0.005% (vol/vol) CO2 under the preexisting conditions.

Nitrogen-Regulated Expression of cmpABCD in Synechococcus Cells Under High-CO2 Conditions.

To promote nitrogen-regulated expression of the cmpABCD genes under high-CO2 conditions, a mutant CMP+ (Fig. (Fig.1)1) was constructed by replacing the promoter of the cmp operon with that of the nirA operon as follows. A 0.59-kbp DNA fragment, carrying nucleotides +1 to +579 of the cmpA-coding region, was amplified by PCR and cloned into pT7Blue T-Vector (Novagen). Two bases of the sense primer used, corresponding to nucleotides −2 and −1 with respect to cmpA initiation codon, had been changed from G and T in the original cmpA sequence to T and C, respectively, to create a BspHI recognition site at the translation start site. After confirmation of nucleotide sequence, the cmpA fragment was excised from the plasmid with BspHI and EcoRI and assembled in pUC19 with a 0.56-kbp HindIII/NcoI fragment of the nirA upstream region. In the resulting plasmid, the nirA upstream region (nucleotides −560 to −1 with respect to the nirA initiation codon) was fused with the cmpA-coding region (nucleotides +1 to +579 with respect to the cmpA initiation codon). A spectinomycin/streptomycin resistance (sper) gene cassette excised from plasmid pRL463 (18) was subsequently ligated between the two BalI sites in the nirA upstream region to replace the 46-bp region extending from nucleotide −368 to −323 with respect to the initiation codon. A 1.6-kbp Eco47III fragment excised from the resulting plasmid, carrying, sequentially, nucleotides −410 to −369 of the nirA upstream region, the sper gene cassette, nucleotides −322 to −1 of nirA upstream region, and nucleotides +1 to +66 of cmpA-coding region, was ligated between nucleotides −143 and +67 of cmpA on a 1.7-kbp Synechococcus DNA fragment that had been cloned separately in pUC19. The resulting plasmid was used to transform the WT strain to spectinomycin resistance through homologous recombination. The transformants were allowed to grow on solid medium supplemented with 15 μg of spectinomycin per ml. After three serial streak-purifications to segregate homozygous mutants (19), genomic DNA was isolated from the selected clones and analyzed by Southern hybridization, using the sper gene cassette as a probe, and PCR to confirm the insertion of the sper gene cassette and the nirA promoter in the cmpA regulatory region, respectively.

Figure 1
Comparison of the structures of the cmp-genomic region in WT and in the M42 (ΔcmpAB::kanr) and CMP+ (PnirA::cmpABCD) mutants of Synechococcus sp. strain PCC7942. The bar above the map shows the probe region used for Northern ...

Measurements of the Initial Rate of HCO3 Uptake After Onset of Light.

Cells were collected by centrifugation as described above, washed twice by recentrifugation and resuspension in the assay buffer (50 mM BTP-HCl, pH 9.0/15 mM NaCl/0.3 mM MgSO4/0.26 mM CaCl2/0.22 mM K2HPO4), which had been sparged with a mixture of N2 and O2 (4:1, vol/vol) for >4 h, and finally suspended in the assay buffer at a chlorophyll (Chl) concentration of 2.9 μg/ml. After incubation under illumination at 30°C for 30 min in a tightly sealed tube, aliquots of 0.39 ml of the cell suspension were transferred to microcentrifuge tubes. NaH14CO3 was added in the dark to the cell suspensions to give a final HCO3 concentration of 100 μM. Immediately after the addition of HCO3, 0.25 ml of the cell suspension was sucked up into a transparent micropipette tip, and HCO3 uptake was started by onset of illumination at 400 μmol of photons m−2[center dot]s−1 provided through optical fibers. The uptake reaction was terminated by rapid filtration of the cells onto a glass filter (GF/B, Whatman) by suction, followed by immediate washing of the filter with 5 ml of the assay buffer, and the radioactivity retained on the filter was measured with a scintillation counter.

Measurements of the Rates of CO2 and HCO3 Uptake During Steady-State Photosynthesis.

Cells were harvested, washed, and suspended in the assay buffer as described above, except that the pH of the assay buffer was 8.2. The steady-state rates of gross CO2 and net HCO3 uptake were measured by a mass spectrometric disequilibruim technique in an aqueous phase-sampling mass spectrometer as described previously (20) under illumination at 300 μmol of photons m−2[center dot]s−1.

Isolation and Analysis of DNA and RNA.

Chromosomal DNA was extracted and purified from the Synechococcus cells as described by Williams (19). Manipulations and analyses of DNA were performed according to standard protocols (21). Total RNA was extracted and purified from Synechococcus cells by the method of Aiba et al. (22). For Northern hybridization analysis, a 0.7-kbp SalI/SphI fragment of cmpC was used as a probe (Fig. (Fig.11).

Immunoblotting Analysis.

Cytoplasmic (plasma) membrane was purified from Synechococcus cells as described (23). Membrane samples amounting to 5 μg of protein were solubilized in the sample buffer for SDS/PAGE (24) at room temperature for 30 min. After gel electrophoresis in the buffer system of Laemmli (24), polypeptides were electrotransferred to a poly(vinylidene difluoride) membrane and allowed to react with IgG against CmpA (8). A goat anti-rabbit IgG-alkaline phosphatase conjugate (Bio-Rad) was used as the second antibody and detected by the color development reaction catalyzed by alkaline phosphatase with nitroblue tetrazolium and 5-bromo-4-chloro-3-indolyl phosphate as substrates.

Other Methods.

Chl and protein were determined according to Mackinney (25) and Lowry et al. (26), respectively.


Expression of cmp Genes in WT and the CMP+ Mutant.

Northern hybridization analysis using a cmpC-specific probe showed that expression of the gene is induced by Ci limitation in the WT cells of Synechococcus sp. PCC 7942 (Fig. (Fig.22A, lanes 1 and 2). The hybridization profile showed a discrete 5.2-kb band preceded by a smaller smeary signal, indicating that the gene is transcribed as a 5.2-kb mRNA, which is rapidly degraded. The 5.2-kb mRNA is close to the calculated size of the cmpABCD gene cluster, 5.1 kb, and probes specific to other cmp genes yielded essentially the same hybridization profiles (not shown), verifying that the cmpABCD genes constitute a low-CO2-inducible operon in the WT strain. Although WT cells did not express the cmpABCD operon under high-CO2 conditions irrespective of the nitrogen conditions tested (Fig. (Fig.22A, lane 1 and Fig. Fig.22B, lanes 1 and 2), the CMP+ cells accumulated a large amount of cmpABCD transcript under high-CO2 conditions when transferred from ammonium-containing medium to nitrate-containing medium (Fig. (Fig.22B, lane 4). The cells accumulated insignificant amounts of cmpABCD transcript when grown with ammonium (Fig. (Fig.22B, lane 3). These results verified that transcription of cmpABCD in CMP+ is under the control of the nirA operon promoter (13, 27). Immunoblot analysis of the cytoplasmic membrane proteins showed that nitrate-grown CMP+ cells accumulated the 42-kDa protein under high CO2 to an amount comparable with that in the low-CO2-induced WT cells (Fig. (Fig.22C, lanes 2 and 4), confirming effective translation and processing from the cmpABCD transcript under high-CO2 conditions. Although minute levels of cmpABCD transcript (Fig. (Fig.22B, lane 3) were detected, ammonium-grown CMP+ cells accumulated small amounts of the 42-kDa protein (Fig. (Fig.22C, lane 3), confirming that the nirA operon promoter is not completely suppressed.

Figure 2
(A) Northern hybridization analysis of total RNA from Synechococcus, showing the effects of CO2 conditions on expression of the cmp operon. Synechococcus cells were grown with NO3 under high-CO2 conditions (2% CO2 in air) and transferred ...

HCO3 Uptake Activity of the CMP+ Mutant.

Fig. Fig.33 shows the time course for HCO3 uptake by WT and CMP+ cells after onset of illumination at pH 9 and 100 μM external HCO3 concentration, under which conditions HCO3, comprising ≈99.8% of Ci in medium, is for practical purposes considered as the Ci species actively transported into the cell. Whereas the WT cells grown under high CO2 on nitrate took up negligible amounts of HCO3 during the first 20 s after illumination (<20 nmol per mg of Chl), the CMP+ cells grown under the same conditions accumulated 260 nmol of HCO3 per mg of Chl. The rate of HCO3 uptake by high-CO2/nitrate-grown CMP+ cells was calculated to be 47 μmol per mg of Chl per h, which corresponded to one-half of that in the low CO2/nitrate-grown WT cells, namely 98 μmol per mg of Chl per h. By contrast, when grown with ammonium, the HCO3 uptake rate of the CMP+ cells was only 20% of that in the nitrate-grown cells and only 10% of the rate in WT cells adapted to low CO2. These results demonstrate that nitrogen-regulated expression of the cmp operon correlates with an elevated capacity to transport low concentrations of HCO3 in the CMP+ mutant under high-CO2 conditions.

Figure 3
Uptake of HCO3 by high-CO2-grown cells (H) of WT ([filled triangle]) and the CMP+ mutant (○, ●) and low-CO2-grown cells ([filled triangle]) of WT (H) in the light. Cells were grown with NH4+ (○) or NO3 (●, ...

Fig. Fig.44A shows the dependence of the rates of O2 evolution on external HCO3 during steady-state photosynthesis of high-CO2-grown cells of CMP+ and WT. In WT cells and ammonium-grown CMP+ cells, the O2 evolution rates showed a saturation-type kinetics with respect to the external HCO3 concentration, with the K1/2 value (the concentration of HCO3 required for the one-half maximal response) being 260 μM and 170 μM, respectively. The O2 evolution rate of nitrate-grown CMP+, on the other hand, showed a biphasic response to external HCO3; the rate sharply increased with increasing external HCO3 up to 30 μM concentration and then gradually increased to reach a maximum level similar to that in WT and ammonium-grown CMP+ cells at ≈1 mM external HCO3 concentration. The K1/2 value for the first phase was 16 μM. These findings show that nitrate-grown CMP+ cells have an efficient mechanism to use low concentrations of external Ci for photosynthesis. When the steady-state rates of net HCO3 and gross CO2 uptake were plotted as functions of external HCO3 (Fig. (Fig.44 B and C), it was clear that the nitrate- and ammonium-grown CMP+ cells differed greatly in their ability to take up low concentrations of HCO3 into the cell. The K1/2 value for HCO3 uptake was 15 μM and 60 μM in the nitrate- and ammonium-grown cells, respectively. These findings demonstrated that induction of cmpABCD genes under high-CO2 conditions led to selective expression of a high-affinity, HCO3 transport activity. The K1/2 value for HCO3 uptake in ammonium-grown CMP+ was smaller than that in WT cells, 120 μM, presumably due to the low-level expression of the cmpABCD genes in the presence of ammonium (Fig. (Fig.22C, lane 3). We therefore conclude that the cmpABCD gene cluster encodes an ABC-type HCO3 transporter, designated BCT1.

Figure 4
The rate of O2 evolution (A), net HCO3 uptake (B), and gross CO2 uptake (C) as a function of the HCO3 concentration in medium during steady-state photosynthesis in WT ([filled triangle]) and the CMP+ mutant (○ and ●). ...

HCO3 Uptake Activity of the cmp Deletion Mutant.

Fig. Fig.55 shows the rates of O2 evolution (A), net HCO3 uptake (B), and gross CO2 uptake (C) of the high-CO2-grown and low-CO2-adapted cells of WT and M42 during steady-state photosynthesis. The high-CO2-grown cells of WT and M42 were essentially the same in their activity to take up CO2 and HCO3 and to photosynthesize over a range of HCO3 concentrations. Incubation of the cells under Ci-limited conditions increased the HCO3 uptake activity in both WT and M42 but in different ways. The K1/2 value for HCO3 uptake in WT cells decreased from 300 μM to 11 μM, similar to previously reported data (28); however, in the M42 mutant, defective in the cmpABCD genes, the K1/2 value declined to only 33 μM. Also, the maximal rate of HCO3 uptake was increased by 50% in WT after incubation under low CO2, but there was no change in the maximal rate of HCO3 uptake in M42 (Fig. (Fig.55B). The capacity for CO2 transport was marginally larger in M42 than in WT after growth under the Ci-limited conditions (Fig. (Fig.55C). The maximum rate of O2 evolution was similar in low CO2-grown WT and M42 cells, but M42 showed a lower affinity for HCO3 (K1/2 = 70 μM) than WT cells (K1/2 = 15 μM). These results are consistent with the loss of BCT1 activity in M42 cells, and at the same time, confirm the existence of a second, low-CO2-inducible, HCO3 transporter in the BCT1-deficient mutant (29). The larger K1/2 value for HCO3 uptake in low-CO2-induced M42 cells indicates that BCT1 has the highest affinity for HCO3 of the HCO3 transport activities present in Synechococcus sp. PCC 7942.

Figure 5
The rate of O2 evolution (A), net HCO3 uptake (B), and gross CO2 uptake (C) as a function of the HCO3 concentration in medium during steady-state photosynthesis in WT (□ and ■) and the M42 mutant ([open triangle] and [filled triangle]). ...


Studies on the cyanobacterial CCM have so far depended on loss-of-function analysis of the properties of mutants defective in specific genes. The approach, however, has limitations in studies of biochemical functions encoded by functionally redundant genes, such as the multiple transporters used in the uptake of Ci. We, therefore, performed a gain-of-function analysis to ascertain the role of cmpABCD. A nitrogen-regulated promoter allowed expression of the genes under high-CO2 conditions (Fig. (Fig.2),2), in which high-affinity Ci transport activities are normally not induced. Measurements of the initial rate of HCO3 uptake after onset of light and of the steady-state rate of HCO3 uptake in the light showed that the selective induction of cmpABCD resulted in expression of high-affinity HCO3 transport activity (Figs. (Figs.33 and and4),4), demonstrating that the gene cluster encodes a high-affinity HCO3 transporter that we have now named BCT1. BCT1 is the first ABC transporter known to transport HCO3 and appears to be the first primary-active HCO3 transporter, although Na+/HCO3 cotransporters and HCO3/anion exchangers have been characterized in mammals.

We previously thought that cmpA was not involved in HCO3 transport on the basis of the presence of inducible Ci transport activities in M42 (8). The present results, obtained from mass spectrometric analysis of the steady-state rates of Ci uptake, confirmed the existence of the inducible CO2 and HCO3-transporting activities in M42, but in accordance with the loss of BCT1, the mutant was impaired specifically in induction of a high-affinity HCO3 uptake mechanism (Fig. (Fig.5).5). These findings indicate that Synechococcus sp. strain PCC7942 has at least two low CO2-inducible HCO3 transporters, with BCT1 having the highest affinity for HCO3. We predict that BCT1 will be of considerable ecological significance in cyanobacteria. The remaining HCO3 transport activity in M42 is presumably predominated by a HCO3 transporter(s) capable of a fast induction response (within 10 min) that is initially independent of transcription–translation events (30).

Recently, a gene (ictB) essential for HCO3 transport has been cloned from a high CO2-requiring mutant of Synechococcus sp. strain PCC 7942 and presumed to encode a HCO3 transporter on the basis of the hydrophobic nature of the deduced protein (5). However, inactivation of ictB practically abolishes induction of high-affinity HCO3 transport activity under low-CO2 conditions (5), meaning that all the low-CO2-inducible HCO3-transporting mechanisms, encoded by cmpABCD and the other(s) remaining in M42, are missing or nonfunctional in the ictB mutant. Therefore, ictB appears to be epistatic to cmpABCD and is unlikely to encode a HCO3 transporter by itself. The essential role of ictB in HCO3 transport suggests that the product of ictB may be involved in other processes, such as the transport of other ion(s) for compensating the large flux of negative electric charge across the plasma membrane during the uptake of HCO3. Further work is required for elucidation of the biochemical function of the product of the ictB gene.

In the nitrate/nitrite transporter of Synechococcus sp. strain PCC 7942, the NrtA protein has been shown to be the substrate- (nitrate and nitrite) binding lipoprotein anchored to the cytoplasmic membrane (12). CmpA is 46.5% identical to NrtA (31) and has a putative signal peptide typical of a lipoprotein (12), suggesting that the protein is a membrane-anchored lipoprotein and functions as the HCO3-binding protein. On the other hand, one of the ATP-binding subunits of the nitrate/nitrite transporter, NrtC, has a distinct C-terminal domain required for ammonium-promoted inhibition of nitrate/nitrite transport (32). Because CmpC also has a C-terminal domain, which is 30% identical to the corresponding domain of NrtC (9), it is inferred by analogy that CmpC has a regulatory role in HCO3 transport. Currently it is unknown what kind of regulation the BCT1 transporter is subject to. Biochemical and molecular biological studies on the CmpA and CmpC proteins are being performed to elucidate the structure–function relationships of the HCO3 transporter.


This work was supported by a Grant-in-aid for Scientific Research (C) (09640768) and a Grant-in-aid for Scientific Research in Priority Areas (A) (09274103) to T. Omata from the Ministry of Education, Science, Sports and Culture, Japan, and a grant on “Research for Future Program” (RFTF97R16001) from the Japanese Society for Promotion of Science (to T. Ogawa). G.D.P. and M.R.B. were supported by the core funding from the Research School of Biological Sciences, Institute of Advanced Studies, Australian National University.


ATP-binding cassette
CO2-concentrating mechanism
inorganic C
wild type


1. Kaplan A, Schwarz R, Lieman-Hurwitz J, Ronen-Tarazi M, Reinhold L. In: The Molecular Biology of Cyanobacteria. Bryant D A, editor. Dordrecht, The Netherlands: Kluwer; 1994. pp. 469–485.
2. Price G D, Sültemeyer D, Klughammer B, Ludwig M, Badger M R. Can J Bot. 1998;76:973–1002.
3. Ogawa T. Proc Natl Acad Sci USA. 1991;88:4275–4279. [PMC free article] [PubMed]
4. Sonoda M, Katoh H, Vermaas W, Schmetterer G, Ogawa T. J Bacteriol. 1998;180:3799–3803. [PMC free article] [PubMed]
5. Bonfil D J, Tarazi-Ronen M, Sültemeyer D, Lieman-Hurwitz J, Schatz D, Kaplan A. FEBS Lett. 1998;430:236–240. [PubMed]
6. Omata T, Ogawa T. Plant Physiol. 1986;80:525–530. [PMC free article] [PubMed]
7. Omata T, Ogawa T, Marcus Y, Friedberg D, Kaplan A. Plant Physiol. 1987;83:892–894. [PMC free article] [PubMed]
8. Omata T, Carlson T J, Ogawa T, Pierce J. Plant Physiol. 1990;93:305–311. [PMC free article] [PubMed]
9. Omata T. In: Research in Photosynthesis. Murata N, editor. III. Dordrecht, The Netherlands: Kluwer; 1992. pp. 807–810.
10. Omata T, Andriesse X, Hirano A. Mol Gen Genet. 1993;236:193–202. [PubMed]
11. Luque I, Flores E, Herrero A. Biochim Biophys Acta. 1994;1184:296–298.
12. Maeda S, Omata T. J Biol Chem. 1997;272:3036–3041. [PubMed]
13. Maeda S, Kawaguchi Y, Ohe T, Omata T. J Bacteriol. 1998;180:4080–4088. [PMC free article] [PubMed]
14. Stanier R Y, Kunisawa R, Mandel M, Cohen-Bazire G. Bacteriol Rev. 1971;35:171–205. [PMC free article] [PubMed]
15. Suzuki I, Kikuchi H, Nakanishi S, Fujita Y, Sugiyama T, Omata T. J Bacteriol. 1995;177:6137–6143. [PMC free article] [PubMed]
16. Samuelsson G, Lönneborg A, Rosenqvist E, Gustafsson P, Öquist G. Plant Physiol. 1985;79:992–995. [PMC free article] [PubMed]
17. Badger M R, Gallagher A. Aust J Plant Physiol. 1987;14:189–201.
18. Elhai J, Wolk C P. Gene. 1988;68:119–138. [PubMed]
19. Williams J G K. Methods Enzymol. 1988;167:766–778.
20. Badger M R, Palmqvist K, Yu J-W. Physiol Plant. 1994;90:529–536.
21. Sambrook J, Fritsch E F, Maniatis T. Molecular Cloning: A Laboratory Manual. 2nd Ed. Plainview, NY: Cold Spring Harbor Lab. Press; 1989.
22. Aiba H, Adhya S, de Crombrugghe B. J Biol Chem. 1981;256:11905–11910. [PubMed]
23. Murata N, Omata T. Methods Enzymol. 1988;167:245–251.
24. Laemmli U K. Nature (London) 1970;227:680–685. [PubMed]
25. Mackinney G. J Biol Chem. 1941;140:315–322.
26. Lowry O H, Rosebrough N J, Farr A L, Randall R J. J Biol Chem. 1951;193:265–275. [PubMed]
27. Suzuki I, Sugiyama T, Omata T. Plant Cell Physiol. 1993;34:1311–1320.
28. Yu J-W, Price G D, Badger M R. Aust J Plant Physiol. 1994;21:185–195.
29. Espie G S, Kandasamy R A. Plant Physiol. 1992;98:560–568. [PMC free article] [PubMed]
30. Sültemeyer D, Klughammer B, Badger M R, Price G D. Plant Physiol. 1998;116:183–192. [PMC free article]
31. Omata T. Plant Cell Physiol. 1991;32:151–157.
32. Kobayashi M, Rodríguez R, Lara C, Omata T. J Biol Chem. 1997;272:27194–27201. [PubMed]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences
PubReader format: click here to try


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


  • Compound
    PubChem Compound links
  • Conserved Domains
    Conserved Domains
    Link to related CDD entry
  • Gene
    Gene links
  • Gene (nucleotide)
    Gene (nucleotide)
    Records in Gene identified from shared sequence links
  • MedGen
    Related information in MedGen
  • Nucleotide
    Published Nucleotide sequences
  • Pathways + GO
    Pathways + GO
    Pathways, annotations and biological systems (BioSystems) that cite the current article.
  • Protein
    Published protein sequences
  • PubMed
    PubMed citations for these articles
  • Substance
    PubChem Substance links
  • Taxonomy
    Related taxonomy entry
  • Taxonomy Tree
    Taxonomy Tree

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...