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Journal of Bacteriology, August 1998, p. 3799-3803, Vol. 180, No. 15
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Photosynthetic Electron Transport Involved in
PxcA-Dependent Proton Extrusion in Synechocystis sp. Strain
PCC6803: Effect of pxcA Inactivation on CO2,
HCO3
, and NO3
Uptake
Masatoshi
Sonoda,1
Hirokazu
Katoh,2
Wim
Vermaas,3
George
Schmetterer,4 and
Teruo
Ogawa1,2,*
Graduate School of Bioagricultural
Sciences1 and
Bioscience
Center,2 Nagoya University, Nagoya 464-01, Japan;
Department of Plant Biology and Center for the Study of
Early Events in Photosynthesis, Arizona State University, Tempe, AZ
85287-16013; and
Institute of Physical
Chemistry, University of Vienna, A-1090 Vienna,
Austria4
Received 9 February 1998/Accepted 20 May 1998
 |
ABSTRACT |
The product of pxcA (formerly known as
cotA) is involved in light-induced
Na+-dependent proton extrusion. In the presence of
2,5-dimethyl-p-benzoquinone, net proton extrusion by
Synechocystis sp. strain PCC6803 ceased after 1 min of
illumination and a postillumination influx of protons was observed,
suggesting that the PxcA-dependent, light-dependent proton extrusion
equilibrates with a light-independent influx of protons. A photosystem
I (PS I) deletion mutant extruded a large number of protons in the
light. Thus, PS II-dependent electron transfer and proton translocation
are major factors in light-driven proton extrusion, presumably mediated
by ATP synthesis. Inhibition of CO2 fixation by
glyceraldehyde in a cytochrome c oxidase (COX) deletion
mutant strongly inhibited the proton extrusion. Leakage of PS
II-generated electrons to oxygen via COX appears to be required for
proton extrusion when CO2 fixation is inhibited. At pH 8.0, NO3
uptake activity was very low in the
pxcA mutant at low [Na+] (~100 µM). At pH
6.5, the pxcA strain did not take up CO2 or NO3 at low [Na+] and showed
very low CO2 uptake activity even at 15 mM Na+.
A possible role of PxcA-dependent proton exchange in charge and pH
homeostasis during uptake of CO2,
HCO3, and NO3 is
discussed.
| |
INTRODUCTION |
Light-induced extrusion of protons
into the medium has been observed in various cyanobacterial strains
(2, 3, 6, 8, 9, 12, 17, 18, 21, 22). Scherer et al.
(17, 18) reported two phases of light-induced proton
extrusion in Anabaena variabilis. The first phase is due to
a light-dependent uptake of CO2, which is converted to
HCO3, and the second phase was considered to
be dependent on ATP and linear photosynthetic electron flow. Both
phases of proton extrusion are specifically stimulated by
Na+. Similar Na+-dependent light-induced proton
extrusion has been observed with Synechococcus and
Plectonema (2, 6, 12). The light-induced proton
extrusion in Plectonema has been assumed to be due to a respiratory electron transport chain localized on the cytoplasmic membrane (2). The physiological significance of the
light-induced proton extrusion is not yet known, and ambiguity remains
whether photosynthetic or respiratory electron transport and whether
cytoplasmic or thylakoid membranes are involved in this reaction.
pxcA (formerly known as cotA) is a homolog of
cemA or ycf10 in chloroplast genomes (7, 8,
21, 22). Light-induced proton extrusion activity was abolished
when pxcA was inactivated in Synechocystis sp.
strain PCC6803 (8, 21) or Synechococcus sp.
strain PCC7942 (22). The pxcA mutants were unable
to grow in low-Na+ medium or in acidic medium. PxcA is
located in the cytoplasmic membrane (21), and the
cemA or ycf10 gene in chloroplast genomes encodes
a chloroplast envelope membrane protein (16). These results
indicate that PxcA is involved in light-induced proton extrusion and
that this protein is essential for cell growth under acidic or low-salt
conditions.
The present study aims to clarify which mode of electron transport is
involved in the light-induced proton extrusion and to determine the
effect of pxcA inactivation on the uptake of
CO2, HCO3, and
NO3. For this reason, pxcA mutants
and strains carrying deletions of genes that code for photosynthetic or
respiratory electron transport components in Synechocystis
sp. strain PCC6803 were analyzed. Measurements of net proton exchange
in the wild-type (WT) and mutant cells with or without electron
acceptors or inhibitors enabled us to conclude that photosystem II (PS
II)-driven electron transport was primarily involved in this reaction.
We have also measured the uptake of CO2,
HCO3, and NO3 in
the WT and pxcA mutant. The results demonstrate that the
PxcA-dependent proton exchange is essential for CO2 uptake
under acidic conditions and for NO3 uptake at
low-Na+ concentrations.
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MATERIALS AND METHODS |
Mutants and growth conditions.
The following mutants were
used in this study: pxcA (previously named M29)
(8), psaAB (PS I-less) (20),
psbDIC/psbDII (PS II-less) (24), and
coxAB (cytochrome c oxidase-less)
(19). WT, pxcA, and coxAB cells were
grown at 30°C in BG-11 medium (23) buffered with 20 mM
N-Tris(hydroxymethyl)methyl-2-aminoethanesulfonic acid (TES)-KOH at pH
8.0; the cultures were aerated with 3% (vol/vol) CO2 in
air. Glucose (5 mM) was added to the above medium for the growth of
psaAB and psbDIC/psbDII mutants. Continuous
illumination was provided by fluorescent lamps at 40-µmol
photosynthetically active radiation/m2/s (400 to 700 nm)
for psaAB cells, which are sensitive to higher light
intensity, and at 100 µmol/m2/s for the other strains.
Measurements of proton exchange and uptake of CO2,
HCO3, and NO3.
Cells harvested by centrifugation were washed twice with 0.2 mM TES-KOH
buffer (pH 8.0) and then suspended in the same buffer at a chlorophyll
concentration of 14 µg/ml (1.4 µg/ml for the psaAB
mutant, which has about sevenfold less chlorophyll on a per-cell basis
[20]). Changes in the pH of the cell suspension (3 ml)
kept at 30°C were monitored by using a pH electrode with a meter
(Inlar 423 and Delta 350; Mettler Toledo, Halstead, United Kingdom).
After each measurement, the signal was calibrated by injecting 10 µl
of 7.5 mM HCl into the cell suspension.
Uptake of CO2 and HCO3 was
measured by the silicone oil-filtering centrifugation method (11,
25). Nitrate uptake was measured as described by Omata et al.
(13). The cells were washed twice with nitrate-free medium
(BG-11 medium minus NaNO3, Na2CO3,
and microelements) buffered with 5 mM MES-KOH at pH 6.5 or with 5 mM
TES-KOH at pH 8.0 and then suspended in the same buffer supplemented with 5 mM KHCO3 to a chlorophyll concentration of 7 µg/ml. NaCl (final concentration, 15 mM) was added to the cell
suspension. The concentration of nitrate was determined with a
Technicon autoanalyzer.
The light source for all the experiments was a 150-W halogen lamp
(MHF-150L; Kagaku Kyoeisha Ltd., Osaka, Japan) equipped
with a glass
fiber. Cells in a sample chamber or in a 1.5-ml Eppendorf
tube were
illuminated by white light from the fiber at an intensity
of 4.0 mmol
of photosynthetically active radiation/m
2/s.
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RESULTS |
Effect of DMBQ on net proton exchange.
The profiles of net
proton exchange measured with the WT and pxcA cells are
shown in Fig. 1. For these measurements,
the cells were suspended in 0.2 mM TES-KOH buffer (pH 8.0) with (Fig.
1D to F) or without (Fig. 1A to C) 2,5-dimethyl-p-benzoquinone (DMBQ). When WT cells suspended in buffer containing 15 mM KCl (Fig. 1A) or
NaCl (Fig. 1B) were illuminated, acidification followed by alkalization
of the medium was observed. The acidification was stimulated by 15 mM
Na+. In contrast, for the pxcA mutant, only
alkalization, not acidification, of the medium was observed upon
illumination (Fig. 1C). It has been reported that alkalization of the
medium is linked to photosynthetic fixation of CO2 produced
by dehydration of HCO3 (10). These
results confirm that Na+-stimulated light-induced proton
extrusion occurs in the WT strain but not in the mutant (8).
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FIG. 1.
Net proton movements in suspensions of WT (A, B, D, and
E) and pxcA (C and F) cells upon switching the light on
(arrow down) and off (arrow up). The cells were suspended in 0.2 mM
TES-KOH buffer (pH 8.0) containing 15 mM KCl (A and D) or NaCl (B, C,
E, and F) in the absence (A to C) and presence (D to F) of 1 mM DMBQ.
The chlorophyll concentration in the cell suspension was 14 µg/ml.
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|
Acidification of the medium was stimulated when WT cells were
illuminated in the presence of DMBQ (Fig.
1D and E). DMBQ can
oxidize
the plastoquinone pool and may be reduced by PS I; hence,
it is an
electron acceptor in photosynthetic electron transport.
Therefore,
proton extrusion is linked to photosynthetic electron
transfer. No net
alkalization followed the acidification on illumination
under these
conditions, due to the absence of photosynthetic CO
2 fixation. The presence of Na
+ showed little effect on the
extent of proton extrusion in the
presence of DMBQ. Figure
1D and E
indicates that the net proton
extrusion does not proceed continuously
in the light but ceases
after 1 min of illumination. After the light
was turned off, an
influx of protons was observed. This suggests that
in the light,
both extrusion and influx of protons occur, reaching an
equilibrium
where there is no net proton exchange, whereas after the
light
is turned off (causing proton extrusion to cease), proton influx
continues for a short time until a new steady-state level is attained.
Both light-induced proton extrusion and postillumination proton
influx
were very low in
pxcA cells in the presence of DMBQ (Fig.
1F).
Net proton exchange in mutants defective in PS I, PS II or
cytochrome c oxidase.
Now that a role of
photosynthetic electron transfer in proton extrusion has been
established, the next question involves the part(s) of photosynthetic
electron transport proton with which extrusion is associated and
whether respiratory electron transfer also plays a role. To address
this question, mutants lacking either PS I, PS II, or cytochrome
c oxidase were investigated. The psaAB (PS
I-less) strain showed Na+-stimulated light-induced proton
extrusion (Fig. 2A and B). On a
per-chlorophyll basis, the amplitude of proton extrusion was two- to
threefold larger than that in WT cells (compare with Fig. 1A and B).
Since about 85% of the chlorophyll in WT Synechocystis sp.
strain PCC6803 is associated with PS I (20), this indicates that PS II-mediated electron transfer can drive a significant amount of
proton extrusion. No proton uptake was observed in the PS I-less mutant
in the light, consistent with the lack of CO2 fixation in
this strain. In the presence of DMBQ, a more extensive acidification
followed by proton uptake was observed (Fig. 2C), similar to what was
seen in WT cells but again with a two- to threefold-higher amplitude on
a per-chlorophyll basis. Thus, PS II-driven electron transport from
water to DMBQ or, to a lesser extent, to oxygen (the latter involving
oxidase[s]) can lead to proton extrusion.
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FIG. 2.
Net proton movement in the suspensions of
psaAB (A to C), psbDIC/psbDII (D and E), and
coxAB (F and G) cells upon switching the light on (arrow
down) and off (arrow up). The cells were suspended in 0.2 mM TES-KOH
buffer containing 15 mM KCl (A) and NaCl (B to G). DMBQ was added prior
to illumination in panels C, E, and F. The chlorophyll concentration in
the cell suspension was 1.4 µg/ml for the psaAB mutant and
14 µg/ml for the psbDIC/psbDII and coxAB
mutants.
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|
A small amount of light-induced proton extrusion was observed when a
cell suspension of the
psbDIC/psbDII strain was illuminated
in the absence of DMBQ (Fig.
2D) but not in its presence (Fig.
2E). The
initial rate of light-induced proton extrusion in the
psbDIC/psbDII strain was about 5% of that in the
psaAB stain on
a per-chlorophyll basis (the rates were 200 and 4,020 µmol/mg
of chlorophyll/h in
psbDIC/psbDII and
psaAB strains, respectively,
in the presence of 15 mM NaCl
but in the absence of DMBQ).
The proton exchange profiles obtained for the
coxAB mutant
in the presence and absence of DMBQ were the same as those obtained
for
WT cells (Fig.
2F and G). Thus, cytochrome
c oxidase is not
essential to proton extrusion under these conditions.
Effect of electron transfer inhibitors and acceptors on proton
exchange.
The results presented thus far imply that electron
transfer involving PS II is a major factor in light-driven proton
extrusion. To further test this, proton extrusion was measured in WT
cells after addition of 3-(3-4-dichlorophenyl)-1,1-dimethylurea (DCMU), a PS II electron transport inhibitor. Indeed, DCMU strongly inhibited the proton extrusion and created a pattern similar to that observed in
the PS-II less mutant (compare Fig. 3B
with Fig. 2D). The proton extrusion was more strongly inhibited by
2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone (DBMIB), an
inhibitor of electron transport at the cytochrome b6/f complex (Fig. 3C). The
light-induced proton extrusion of WT cells in the presence of DMBQ was
completely inhibited by DCMU (Fig. 3D and E); addition of DBMIB
resulted in partial inhibition (Fig. 3F). Addition of DCMU during
illumination in the presence of DMBQ caused influx of protons into the
cells, and no postillumination proton influx was observed on subsequent
removal of the light source (data not shown).
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FIG. 3.
Effect of DMBQ, PNDA, DCMU, and DBMIB on net proton
movements in WT Synechocystis cells. The light was switched
on (arrow down) and off (arrow up) as indicated. The cells were
suspended in 0.2 mM TES-KOH buffer (pH 8.0) containing 15 mM NaCl. DMBQ
(final concentration, 1 mM) (D to E), PNDA (3 mM) (G to I), DCMU (20 µM) (B, E, and H), and DBMIB (10 µM) (C, F, and I) were added as
indicated. All additions were done prior to illumination.
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Addition of
p-nitrosodimethylaniline (PNDA), a PS I electron
acceptor (
1), had little effect. However, if both PNDA and
DCMU were added, the amount of proton extrusion was somewhat greater
than when DCMU alone was added (Fig.
3B and H). DBMIB strongly
inhibited the proton extrusion in the presence of PNDA (Fig.
3I).
These
results indicate that the extrusion of protons was abolished
when both
water splitting and the cytochrome
b6/
f complex were
inhibited. However,
electron transport from water to DMBQ, and,
to a lesser extent, from
the intracellular reductants to electron
acceptors via PS I and/or PS
I-dependent cyclic electron flow
energizes proton extrusion.
To test the hypothesis that alkalization is driven by
HCO
3 utilization, photosynthetic
CO
2 fixation was inhibited by glyceraldehyde
(GA)
treatment. This treatment reduced the rate of alkalization
in both the
WT and
coxAB cells (Fig.
4A,
B, D, and E), indicating
that OH
produced as a result of
bicarbonate utilization is extruded in
the light. Interestingly, GA did
not affect the light-induced
proton extrusion in the WT strain (Fig.
4A
and B) but had a strong
inhibitory effect on proton extrusion in the
coxAB strain (Fig.
4D and E). The GA inhibition was relieved
by addition of DMBQ
(Fig.
4F). A similar result was obtained with the
WT strain when
5 mM KCN was added (Fig.
4G to I). At this
concentration, KCN
inhibits both photosynthetic CO
2
fixation and oxidase activity.
Therefore, in the absence of
photosynthetic CO
2 fixation, electron
flow to oxygen via
cytochrome
c oxidase is essential for proton
extrusion. If
this electron flow cannot occur, the quinone pool
may be overreduced
and continuous electron transfer cannot occur.
However, if DMBQ is
added, PS II-mediated electron transfer can
resume and proton extrusion
is observed.
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FIG. 4.
Effect of GA, KCN, and DMBQ on net proton movements
involving WT (A to C and G to I) and coxAB (D to F) cells of
Synechocystis. The light was switched on (arrow down) and
off (arrow up). The cells were suspended in 0.2 mM TES-KOH buffer (pH
8.0) containing 15 mM NaCl at a chlorophyll concentration of 14 µg/ml. GA (final concentration, 20 mM) (B, C, E, and F) and KCN (5 mM) (H and I) were added prior to illumination and DMBQ (1 mM) (C, F,
and H) was added in the dark to the cell suspensions after the profiles
in the presence of the inhibitors were obtained.
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Effect of Na+ and pH on the uptake of CO2,
HCO3, and NO3 in WT
and pxcA strains.
Protons are produced during the
transport of CO2 and are consumed when
NO3 is reduced to NH4 via
NO2 or when HCO3 is
converted to CO2. Cells have a mechanism to maintain
homeostasis with respect to the intracellular pH and electroneutrality
during these processes. To test whether the PxcA-dependent proton
exchange is involved in maintaining this homeostasis, the uptake of
CO2, HCO3, and
NO3 was monitored as a function of the
activity of proton exchange. For this purpose, the uptake of
CO2, HCO3, and
NO3 in the WT and the pxcA strains
was measured at pH 8.0 and 6.5 in the presence of a normal
concentration of NaCl (15 mM, close to the concentration in BG-11
medium) or KCl (15 mM) with a low contaminating concentration of
Na+ (~100 µM Na+). As reported previously
(5), HCO3 uptake was high at the
normal Na+ concentration and low at the low Na+
concentration in the WT and the pxcA strains (Fig.
5, middle row). Thus, pxcA
inactivation did not affect the HCO3 uptake.
At the low Na+ concentration, the
NO3 uptake was very low in the
pxcA strain at pH 8.0 and was zero at pH 6.5 (bottom rows).
At the normal Na+ concentration, no significant effect of
pxcA inactivation was observed on CO2 and
NO3 uptake at pH 8.0 but CO2
uptake activity was reduced significantly at pH 6.5 (top and bottom
rows). No CO2 uptake was observed in the mutant at pH 6.5 in the presence of a low Na+ concentration. It is evident
that the inactivation of pxcA strongly affected the
CO2 uptake under acidic conditions and the
NO3 uptake at low Na+
concentrations.
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FIG. 5.
Rates of CO2,
HCO3, and NO3
uptake in WT and pxcA cells of Synechocystis at
pH 8.0 and pH 6.5 in the presence of 15 mM NaCl (N-Na+) or
KCl (L-Na+).
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DISCUSSION |
The results presented here demonstrate that proton extrusion is
driven by PS II coupled to the cytochrome
b6/f complex (Fig. 1 to 3). Some
proton extrusion can also be driven by PS I. PxcA is an important
factor in mediating this proton extrusion. The question now is how this
proton extrusion occurs. First, it is unlikely that protons produced by
PS II and the cytochrome b6/f complex
are directly extruded into the medium, since the lumen and the
periplasmic space are presumed to be two different compartments. In addition, protons pumped by these complexes should lead to ATP
synthesis and should not be "wasted" by extrusion. Therefore, an
energy carrier would be required. ATP seems to be the only candidate
for such a carrier that energizes the proton extrusion system; NADPH is
not a candidate, because the PS II electron transfer is effective in
causing proton extrusion.
The activity of proton extrusion appears to be correlated with the
activity of photosynthetic water splitting and electron transport
through the cytochrome b6/f complex;
both of these processes produce a proton gradient across the thylakoid
membrane and thereby can lead to the generation of ATP. This supports
the view that the PxcA-dependent proton extrusion is energized by ATP.
PxcA does not have an ATP-binding motif and therefore probably is
unable to hydrolyze ATP by itself. PxcA may be a regulator of an
ATP-dependent proton extrusion pump, and the pump activity is very low
in the absence of PxcA.
Besides this PxcA-dependent proton exchange system, cyanobacterial
cells possess a Na+/H+ antiport system
(14). In fact, the genome of Synechocystis sp.
strain PCC6803 contains five genes resembling those coding for
Na+/H+ antiporters (4). Two of these
gene products contain an ATP-binding motif. It is possible that these
gene products are involved in PxcA-dependent proton exchange.
The results presented in Fig. 5 indicate that inactivation of
pxcA affects the uptake of CO2 and
NO3. Recently, Rolland et al. reported that
inactivation of cemA affects the uptake of inorganic carbon
in the chloroplast of Chlamydomonas (15). These
results obtained with Synechocystis and
Chlamydomonas strongly suggest that cemA and
pxcA have the same function in chloroplasts and
cyanobacterial cells, respectively.
Based on the results obtained, we propose a working hypothesis
involving two complementary proton exchange systems, one of which
depends on PxcA, to explain the growth characteristics and inorganic
carbon and nitrate uptake of the WT and pxcA strains. This
hypothesis has the following features. (i) PxcA-dependent and
PxcA-independent proton exchange systems play essential roles in
maintaining homeostasis with respect to the intracellular pH and
electroneutrality. The proton exchange catalyzed by both systems is
stimulated by Na+. (ii) Both systems are essential to
growth and CO2 transport at pH 6.5, but the
PxcA-independent system alone is sufficient at pH 8 when the activity
is high at the normal Na+ concentration. However, both
systems are required even at this alkaline pH when the activity of each
system is low at the low Na+ concentration. (iii) At the
low Na+ concentration, NO3 uptake
requires the PxcA-dependent system. However, when PxcA-independent proton exchange is active at the normal Na+ concentration,
the PxcA-dependent system is not required for NO3 uptake. (iv) Uptake of
HCO3 requires a high activity of
PxcA-independent proton exchange at the normal Na+
concentration in both WT and pxcA cells.
Proton exchange catalyzed by the PxcA-independent system should be
observed as the pH of the suspension medium of pxcA cells changes. The slow alkalization observed with pxcA cells in
the light may be due to proton influx by the PxcA-independent system; it is also possible that rapid influx and efflux of protons via the
PxcA-independent system occur with a small net proton movement that
cannot be measured by the pH electrode used in this study.
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ACKNOWLEDGMENTS |
This study was supported by a Grant-in-Aid for Scientific
Research (grant 09640767) from the Ministry of Education, Science, Sports and Culture of Japan and by grants from the New Energy and
Industrial Technology Development Organization (NEDO) of Japan and from
the Human Frontier Science Program.
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FOOTNOTES |
*
Corresponding author. Mailing address: Bioscience
Center, Nagoya University, Chikusa-ku, Nagoya 464-8601, Japan. Phone:
81-52-789-5215. Fax: 81-52-789-5214. E-mail:
h44975a{at}nucc.cc.nagoya-u.ac.jp.
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REFERENCES |
| 1.
|
Elstner, E. F., and H. Zeller.
1978.
Bleaching of p-nitrosodimethylaniline by photosystem 1 of spinach lamellae.
Plant Sci. Lett.
13:15-20.
|
| 2.
|
Hawkesford, M. J.,
P. Rowell, and W. D. P. Stewart.
1963.
Energy transduction in cyanobacteria, p. 199-218.
In
G. C. Papageorgiou, and L. Packer (ed.), Photosynthetic prokaryotes: cell differentiation and function. Elsevier, Amsterdam, The Netherlands.
|
| 3.
|
Hinrichs, I.,
S. Scherer, and P. Boger.
1985.
Two different mechanisms of light induced proton efflux in the blue-green alga Anabaena variabilis.
Physiol. Veg.
23:717-724.
|
| 4.
|
Kaneko, T.,
S. Sato,
H. Kotani,
A. Tanaka,
E. Asamizu,
Y. Nakamura,
N. Miyajima,
M. Hirosawa,
M. Sugiura,
S. Sasamoto,
T. Kimura,
T. Hosouchi,
A. Matsuno,
A. Muraki,
N. Nakazaki,
K. Naruo,
S. Okumura,
S. Shimpo,
C. Takeuchi,
T. Wada,
A. Watanabe,
M. Yamada,
M. Yasuda, and S. Tabata.
1996.
Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions.
DNA Res.
3:109-136[Abstract].
|
| 5.
|
Kaplan, A.,
R. Schwarz,
J. Lieman-Hurwitz,
M. Ronen-Tarazi, and L. Reinhold.
1994.
Physiological and molecular studies on the response of cyanobacteria to changes in the ambient inorganic carbon concentration, p. 469-485.
In
D. A. Bryant (ed.), The molecular biology of cyanobacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands.
|
| 6.
|
Kaplan, A.,
S. Scherer, and M. Lerner.
1989.
Nature of the light-induced H+ efflux and Na+ uptake in cyanobacteria.
Plant Physiol.
89:1220-1225[Abstract/Free Full Text].
|
| 7.
|
Katoh, A.,
K. S. Lee,
H. Fukuzawa,
K. Ohyama, and T. Ogawa.
1996.
A cemA homologue essential to CO2 transport in the cyanobacterium, Synechocystis PCC6803.
Proc. Natl. Acad. Sci. USA
93:4006-4010[Abstract/Free Full Text].
|
| 8.
|
Katoh, A.,
M. Sonoda,
H. Katoh, and T. Ogawa.
1996.
Absence of light-induced proton extrusion in cotA-less mutant of Synechocystis sp. strain PCC6803.
J. Bacteriol.
178:5452-5455[Abstract/Free Full Text].
|
| 9.
|
Lockau, W., and S. Pfeffer.
1982.
A cyanobacterial ATPase distinct from the coupling factor of photophosphorylation.
Z. Naturforsch. Sect. C
37:658-664.
|
| 10.
|
Miller, A. G., and B. Colman.
1980.
Active transport and accumulation of bicarbonate by a unicellular cyanobacterium.
J. Bacteriol.
143:1253-1259[Abstract/Free Full Text].
|
| 11.
|
Ogawa, T.
1991.
A gene homologous to the subunit-2 gene of NADH dehydrogenase is essential to inorganic carbon transport of Synechocystis PCC6803.
Proc. Natl. Acad. Sci. USA
88:4275-4279[Abstract/Free Full Text].
|
| 12.
|
Ogawa, T., and A. Kaplan.
1987.
The stoichiometry between CO2 and H+ fluxes involved in the transport of inorganic carbon in cyanobacteria.
Plant Physiol.
83:888-891[Abstract/Free Full Text].
|
| 13.
|
Omata, T.,
M. Ohmori,
N. Arai, and T. Ogawa.
1989.
Genetically engineered mutant of the cyanobacterium Synechococcus PCC7942 defective in nitrate transport.
Proc. Natl. Acad. Sci. USA
86:6612-6616[Abstract/Free Full Text].
|
| 14.
|
Ritchie, R. J.
1992.
Sodium transport and the origin of the membrane potential in the cyanobacterium Synechococcus R-2 (Anacystis nidulans) PCC7942.
J. Plant Physiol.
139:320-330.
|
| 15.
|
Rolland, N.,
A.-J. Dorne,
G. Amoroso,
D. F. Sultemeyer,
J. Joyard, and J.-D. Rochaix.
1997.
Disruption of the plastid ycf10 open reading frame affects uptake of inorganic carbon in the chloroplast of Chlamydomonas.
EMBO J.
16:6713-6726[Medline].
|
| 16.
|
Sasaki, Y.,
K. Sekiguchi,
Y. Nagano, and R. Matsuno.
1993.
Chloroplast envelope protein encoded by chloroplast genome.
FEBS Lett.
316:93-98[Medline].
|
| 17.
|
Scherer, S.,
I. Hinrichs, and P. Boger.
1986.
Effect of monochromatic light on proton efflux of the blue-green alga Anabaena variabilis.
Plant Physiol.
81:939-941[Abstract/Free Full Text].
|
| 18.
|
Scherer, S.,
H. Riege, and P. Boger.
1988.
Light-induced proton release by the cyanobacterium Anabaena variabilis: dependence on CO2 and Na+.
Plant Physiol.
86:769-772[Abstract/Free Full Text].
|
| 19.
|
Schmetterer, G.,
D. Alge, and W. Gregor.
1994.
Deletion of cytochrome c oxidase genes from the cyanobacterium Synechocystis sp. PCC6803: evidence for alternative respiratory pathways.
Photosynth. Res.
42:43-50.
|
| 20.
|
Shen, G.,
S. Boussiba, and W. F. J. Vermaas.
1993.
Synechocystis sp. PCC6803 strains lacking photosystem I and phycobilisome function.
Plant Cell
5:1853-1863[Abstract].
|
| 21.
|
Sonoda, M.,
K. Kitano,
A. Katoh,
H. Katoh,
H. Ohkawa, and T. Ogawa.
1997.
Size of cotA and identification of the gene Product in Synechocystis sp. strain PCC6803.
J. Bacteriol.
179:3845-3850[Abstract/Free Full Text].
|
| 22.
|
Sonoda, M.,
H. Katoh,
H. Ohkawa, and T. Ogawa.
1997b.
Cloning of cotA gene of Synechococcus PCC7942 and complementation of a cotA-less mutant of Synechocystis PCC6803 with chimeric genes of the two strains.
Photosynth. Res.
54:99-105.
|
| 23.
|
Stanier, R. Y.,
R. Kunisawa,
M. Mandel, and G. Cohen-Bazire.
1971.
Purification and properties of unicellular blue-green algae (order Chroococcales).
Bacteriol. Rev.
35:171-205[Free Full Text].
|
| 24.
|
Vermaas, W. F. J.,
J. Charit, and B. Eggers.
1990.
System for site-directed mutagenesis in the psbD1/C operon of Synechocystis sp. PCC6803, p. 231-238.
In
M. Baltscheffsky (ed.), Current research in photosynthesis, vol. 1. Kluwer Academic Publishers, Dordrecht, The Netherlands.
|
| 25.
|
Volokita, M.,
D. Zenvirth,
A. Kaplan, and L. Reinhold.
1984.
Nature of the inorganic carbon species actively taken up by the cyanobacterium Anabaena variabilis.
Plant Physiol.
76:599-602[Abstract/Free Full Text].
|
Journal of Bacteriology, August 1998, p. 3799-3803, Vol. 180, No. 15
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
