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Plant Physiol, March 2000, Vol. 122, pp. 731-736
Differential Expression of Photosynthesis and Nitrogen Fixation
Genes in the Cyanobacterium Plectonema boryanum
Hari S.
Misra* and
Rakesh
Tuli
Molecular Biology and Agriculture Division, Bhabha Atomic Research
Centre, Trombay, Mumbai 400 085, India (H.S.M.); and National Botanical
Research Institute, Rana Pratap Marg, Lucknow 226 001, India (R.T.)
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ABSTRACT |
The filamentous non-heterocystous
cyanobacterium Plectonema boryanum fixes dinitrogen at a
high rate during microaerobic growth in continuous illumination by
temporal separation of oxygen-evolving photosynthesis and
oxygen-sensitive dinitrogen fixation. The onset of nitrogen fixation is
preceded by a depression in photosynthesis that establishes a
sufficiently low level of dissolved oxygen in the growth medium. A
several-fold reduction in the level of transcripts coding for
phycocyanin (cpcBA) and the chlorophyll a
binding protein of photosystem II (psbC) and
psbA accompanied the depression in photosynthetic oxygen
evolution. Unlike most of the other organisms examined to date, in
P. boryanum, psbC and psbD do
not appear to be co-transcribed. The psbC transcripts were down-regulated several fold, while the psbD
transcript declined marginally during the nitrogen fixation phase. A
decrease in dissolved oxygen and a dramatic increase in the level of
nifH transcripts and the enzyme activity of nitrogenase
were characteristic of the nitrogen fixation phase. The level of
transcript for glnA, which encodes glutamine synthetase,
was not altered. Reciprocal regulation of gene expression was well
orchestrated with the alternating cycles of photosynthesis and nitrogen
fixation in P. boryanum.
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INTRODUCTION |
Several cyanobacteria have the unique ability to conduct both
oxygenic photosynthesis and oxygen-sensitive dinitrogen fixation. Heterocystous cyanobacteria protect nitrogenase and the related redox
machinery from damage by intracellular oxygen by carrying out nitrogen
fixation in morphologically and physiologically differentiated cells
called heterocysts (Haselkorn, 1978 ; Wolk et al., 1994; Böhme, 1998). Photosynthesis takes place simultaneously in
spatially separated vegetative cells. Unicellular and filamentous,
non-heterocystous diazotrophic cyanobacteria do not differentiate
morphologically distinguishable cells. They overcome the problem of
oxygen by fixing dinitrogen either during the dark phase of growth or
in light at a time when photosynthesis is inhibited (Mitsui et al., 1987; Bergman et al., 1997).
The regulation of gene expression during temporal separation of
photosynthesis and nitrogen fixation under diazotrophic growth of
non-heterocystous cyanobacteria has not been studied in detail. The
reciprocal transcription of petF and fdxH genes
in response to nitrogen status under non-diazotrophic conditions has
been reported in P. boryanum. (Schrautemeier et al., 1994).
The rhythmic expression of nifH and other nif
genes during diazotrophic growth has been reported in a unicellular
N2-fixing cyanobacterium,
Synechococcus sp. RF-1, and was shown to be regulated by the
circadian clock (Huang and Chow, 1990; Huang et al., 1999).
The filamentous non-heterocystous cyanobacterium P. boryanum
can be grown with doubling time of around 60 h in nitrogen
starvation conditions by inducing diazotrophy by bubbling an anaerobic
gas mixture in the presence of continuous light (Rai et al., 1992; Misra and Tuli, 1993). Under such growth conditions, the cyanobacterium shows reciprocal, alternating cycles of nitrogen fixation (N-phase) and
photosynthesis (P-phase) (Stewart and Lex, 1970; Misra and Tuli, 1993).
In this report, we examine the organization and expression of some of
the important genes involved in nitrogen fixation and photosynthesis
during the alternating cycles of carbon dioxide fixation and dinitrogen
fixation in P. boryanum.
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MATERIALS AND METHODS |
Analytical and Molecular Biology Reagents
The analytical reagents used in this study were obtained from
Merck (Mumbai, India) and Sigma-Aldrich (St. Louis). Molecular biology
reagents were obtained from Sigma-Aldrich, Life Technologies/Gibco-BRL (Cleveland), and Sisco Research Laboratory (Mumbai, India). All enzymes
and kits were obtained from Amersham-Pharmacia Biotech (Uppsala),
Boehringer Mannheim (Mannheim, Germany), New England Biolabs (Beverly,
MA), and Bangalore Genei Pvt. Ltd. (Bangalore, India). Radionucleotides
were obtained from the Board of Radiation and Isotope Technology
(Mumbai, India). Positively charged nylon membranes from
Amersham-Pharmacia Biotech was used in capillary transfer of DNA and RNA.
Organism and Growth Conditions
Plectonema boryanum strain UTEX 594 was obtained from
the University of Texas collection. A dinitrogen-fixing,
photoautotrophic culture was established by continuous bubbling of a
N2 and CO2 mixture (19:1)
in nitrogen-deficient BG110 (Rippka et al., 1979) medium. The inoculum was grown under aerobic conditions in BG11 medium
and used to induce diazotrophic growth in a 15-L fermenter vessel under
continuous illumination (light intensity 8,000 lux), as
previously described (Misra and Tuli, 1994). On-line dissolved oxygen
was monitored with a Clark-type oxygen electrode installed in the
fermenter vessel as previously described (Misra and Tuli, 1993; Misra,
1999). Nitrogenase was estimated by the acetylene reduction assay in
the anaerobic gas phase as previously described (Misra and Tuli, 1993).
Chlorophyll was extracted in methanol and estimated (Mackiney, 1941).
Isolation of DNA and Southern Hybridization
Total DNA from P. boryanum was prepared according to a
modified protocol of Felkner and Barnum (1988). The cyanobacterial culture grown to mid-exponential phase in BG11 medium was harvested and
washed in 10 mM Tris-HCl (pH 8.0) and 1 mM EDTA. One gram of cell pellet was suspended in
4 mL of Suc buffer (50 mM Tris-HCl, pH 8.0, 100 mM EDTA, and 25% [w/v] Suc). Lysozyme was
added to a final concentration of 5 mg/mL and incubated for 1 h at
37°C .The suspension was treated with proteinase K (100 µg/mL) and incubated at 37°C in the presence of 1.0% (w/v) SDS until it
become clear. The cleared lysate was extracted with phenol and
chloroform. The subsequent steps were as described previously (Vachhani
et al., 1993). Total DNA (5.0 µg) was digested with restriction
enzymes, treated for 30 min at 37°C with DNase-free RNase (50 µg/mL), and resolved on 1.0% (w/v) agarose. DNA fragments
were transferred to positively charged nylon membranes. The DNA probes
used in this study are given in Table I.
The appropriate restriction fragments were cut from respective plasmids
and eluted from low-melting-point agarose. Probes were labeled using a
kit from Boehringer Mannheim/Roche and following the manufacturer's
protocol. Prehybridization and hybridization were carried out as
described by Sambrook et al. (1989).
Isolation of RNA and Hybridization
Total RNA was isolated from aliquots of the cyanobacterial
culture, as previously described (Chomczynski and Sacchi, 1987), with
some modifications. The cells were harvested at 4°C, and washed
pellets were immediately frozen at  70°C and then thawed. A high
concentration of guanidinium thiocyanate (5 M) was used and
cells were broken by vortexing with acid-washed sterile glass beads
(0.45-0.60 mm diameter) as described previously (Mann et al., 1991).
The RNA pellet was washed with 3 M sodium acetate (pH
5.6-6.3) to reduce DNA contamination in the preparation. The RNA
concentration was determined spectrophotometrically and used in
northern- and dot-blot hybridization (Sambrook et al., 1989). Detection
of signal and quantitation of probes hybridized to specific RNA on
dot-blot filters were done using a phosphor imager (Molecular Dynamics,
Sunnyvale, CA).
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RESULTS |
Temporal Separation of Photosynthesis and Dinitrogen Fixation
As described in our earlier studies (Misra and Tuli, 1993, 1994),
a rapid photoautotrophic growth of P. boryanum under
nitrogen starvation conditions could be achieved by bubbling the
culture with an anaerobic gas mixture in continuous light. A fall in
photosynthesis (monitored as light-dependent oxygen evolution) and a
concomitant rise in dinitrogen fixation (monitored by acetylene
reduction activity) commenced about 15 h after the onset of
anaerobic bubbling (Fig. 1). At the onset
of nitrogenase activity, the steady-state dissolved oxygen in the
medium fell below 15 µM due to a decline in
photosynthetic oxygen evolution. After the peak of the N-phase, photosynthetic oxygen evolution (P-phase) was switched on and the
steady-state dissolved oxygen in the medium increased rapidly to 35 to
70 µM (Misra and Tuli, 1993). The cycle of the
two reciprocal phases was repeated throughout diazotrophic growth of
the organism. The aliquots were withdrawn anaerobically at the peak of
the N-phase and the P-phase to prepare RNA for northern- and dot-blot
hybridization experiments.
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Figure 1.
Alternating cycles of nitrogen fixation (N1 and
N2) and photosynthesis (P1 and P2) in P. boryanum strain
UTEX 594 growing in continuous light under nitrogen-fixing conditions.
Acetylene reduction activity ( ) and light-dependent oxygen evolution
( ) were monitored in the medium during the first two cycles.
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Specificity of Gene Probes and Copy Number
The DNA probes (Table I) used in this study were from heterologous
cyanobacterial species and showed fairly high specificity of
hybridization with the DNA from P. boryanum. As shown in
Figure 2, all bands were clear and
distinct when hybridization was carried out at 65°C, except
cpc, which was hybridized at 55°C.
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Figure 2.
Southern-blot analysis of P.
boryanum strain UTEX 594 DNA. Total DNA was digested with
HindIII (lanes 1) and EcoRI (lanes 2) and
hybridized with genes probe for psbA,
psbD, psbC, cpcBA, and
nifH. Sizes of the major hybridizing fragments are given
on the sides of the lane (in kb). All hybridizations were carried out
at 65°C, except for cpc at 55°C.
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Among the genes encoding some of the major proteins of photosystem II
(PSII), the results presented in Figure 2 suggest the presence of at
least two copies of psbA and psbD each in
P. boryanum and a single copy of psbC. The probe
for cpcBA hybridized strongly to a (3.2-kb)
HindIII and an (2.4-kb) EcoRl fragment and weakly to a few additional fragments. The multiple bands obtained with the
cpc gene probe could be due to partial homology among
phycobiliprotein genes and/or multiple copies of the phycocyanin genes,
as reported in other cyanobacteria (Grossman et al., 1993).
Southern-blot analysis with nifH (Fig. 2), nifD,
and nifK (data not included) gene probes suggested the
presence of these genes in single copy in P. boryanum, which
agrees with earlier results for this organism (Apte and Thomas, 1987).
That study showed that, unlike heterocystous cyanobacteria, the
nifHDK operon is contiguous and present as a 3.6-kb
EcoRI fragment on the chromosome of P. boryanum
strain 594. Nucleotide sequence and differential expression of
nifH have also been shown in a different strain of P. boryanum strain M101 (Fujita et al., 1991). A gene representative
of nitrogen metabolism, glnA, was also present in single
copy in P. boryanum (data not included).
Level of Transcripts during Temporal Separation of Photosynthesis
and Nitrogen Fixation
nif Genes
The abundance of transcripts for the above genes was determined by
dot-blot hybridization of total RNA prepared from the aliquots drawn
during two successive N- and P-phases (i.e. N1, P1, N2, and P2) as
shown in Figure 1. The blots were hybridized to a 23S r DNA
(rrn) gene probe to ascertain that equal amounts of total RNA were blotted uniformly (Fig. 3).
Hybridization of the dot blots with the nifH gene probe
showed that the nif transcripts were present at a high level
during the N-phase and nearly disappeared during the P-phase (Fig. 3).
On northern blots (Fig. 4), the
predominant nifH transcript was the 1.4-kb form, while
less-intense bands, apparently representing the multicistronic
transcripts nifHD and nifHDK, were seen at
approximately 2.6 and 4 kb, respectively. Multiple nif
transcripts produced by termination events at the ends of the
nifH and nifD genes have been previously reported in P. boryanum (Fujita et al., 1991) and heterocystous
cyanobacteria (Haselkorn et al., 1986). All three transcripts in
P. boryanum disappeared nearly completely during the
P-phase. On dot-blots, the level of nifH transcripts showed
rhythmic changes that were completely in agreement with the appearance
and disappearance of the acetylene reduction activity of nitrogenase
(Fig. 1). Such a pattern was not followed by the glnA
transcripts encoding Gln synthetase, the key enzyme involved in the
assimilation of newly fixed nitrogen (Fig. 3). In agreement with the
unchanged level of the transcript, the level of Gln synthetase enzyme
activity in crude extracts remained unaltered during the N- and
P-phases (data not shown).
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Figure 3.
Dot-blot analysis of the total RNA isolated from a
P. boryanum culture. Aliquots were drawn during the
first two nitrogen fixation (N1 and N2) and photosynthesis (P1 and P2)
phases, as shown in Figure 1. The RNA samples blotted in quadruplicate
from each phase were hybridized with rrn,
nifH, glnA, cpcBA,
psbA, psbD, and psbC gene
probes. All hybridizations were carried out at 65°C except that for
cpc, which was at 60°C.
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Figure 4.
Northern-blot analysis of total RNA isolated from
diazotrophic cultures of P. boryanum during the first
nitrogen fixation (N) and photosynthesis (P) phases. The probes were
nifH, cpcBA, psbA,
psbD, and psbC. Sizes of the hybridizing
transcripts are given on the lanes in kb. All hybridizations were
carried out at 65°C, except that for cpc, which was at
60°C.
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cpcBA Genes
Among the genes related to photosynthesis, the transcripts for
 - and  -subunits of phycocyanins showed a remarkable decline in
the N-phase and a rapid 5- to 8-fold increase in the subsequent P-phase
in dot-blot hybridization (Fig. 3). The results of northern hybridization (Fig. 4) agreed with those of dot-blots in showing stronger signals of hybridization with RNA prepared from the culture in
the P-phase. Transcripts of all three sizes, i.e. 4, 2.4, and 1.6 kb,
proportionately declined during the N1-phase. The 2.4-kb transcript was
most prominent during both the growth phases. The relative depression
in the level of all three transcripts was higher during the N-phase,
i.e. immediately after transfer of the culture to the
nutrient-deficient medium, compared with that during the subsequent
N-phases.
Photosystem II Reaction Center Component Genes
The level of psbA transcript in the P-phase was
distinctly higher than that in the preceding N-phase (Fig. 3). Since
there are multiple genes for psbA (Fig. 2) in P. boryanum, northern hybridization was conducted to examine the
sizes of the transcripts. An RNA band of 1.5 kb in the N-phase and two
RNA bands of 1.5 and 0.6 kb in the P-phase hybridized with the
psbA gene probe (Fig. 4). The intensity of the 1.5-kb band
was higher in the P-phase than in the N-phase and agrees with the
results of dot-blot hybridization. The psbA transcript
declined to a very low level during the N1-phase, i.e. immediately
after the culture was inoculated into nitrogen-deficient medium. During
the next N-phase, i.e. N2, the decrease in the level of psbA
was not as much as that in N1, and was insignificant compared with that
in the P2-phase (Fig. 3).
Unlike psbA, the steady-state level of transcripts for
psbD declined marginally (10%-20%) as the culture shifted
from the P-phase to the N-phase (Fig. 3). Northern hybridization with
the psbD gene probe showed the presence of two transcripts
of 2.8 and 1.6 kb (Fig. 4) during both the P-phase and the N-phase. The level of both transcripts in the N1 phase was about 80% of that in the
P1 phase. Unlike cpcBA and psbA, the decline in
psbD transcript in N1 was not significantly more than that
in the N2 phase. Northern hybridization with an internal
psbC gene probe showed its hybridization with the 2.8-kb
RNA, as did psbD (Fig. 4). However, results from dot-blot
hybridization (Fig. 3) and northern hybridization (Fig. 4) demonstrated
a cyclic 70% to 90% reduction in the level of 2.8-kb transcript
hybridized with psbC probe in the N-phase compared with the
P-phase. The smaller 1.6-kb transcript homologous to psbD
did not hybridize with psbC. A several-fold decline in
hybridization of the 2.8-kb transcript to the psbC gene
probe and only a marginal decline in its hybridization to the
psbD gene probe in the N-phase was observed even when the
same blot was hybridized after stripping the previous probe. As in the
case of cpcBA and psbA, the transcript of
psbC declined to a much lower level during the N-phase
immediately after the culture was transferred to conditions that
permitted nitrogen fixation compared with the subsequent N-phases.
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DISCUSSION |
Temporal separation of photosynthesis and dinitrogen fixation
during growth in continuous light has been reported in P. boryanum (Rai et al., 1992; Misra and Tuli, 1994) and in a few
other filamentous and unicellular non-heterocystous cyanobacteria
(Bergman et al., 1997). Most of the non-heterocystous cyanobacteria
accumulate a high level of carbon reserves such as glycogen (Mullineaux
et al., 1980; Schneegurt et al., 1994) during the light phase, which are mobilized to provide reductant and ATP to fix dinitrogen during the
dark phase when grown in a diurnal light-dark regime. A depression in
photosynthesis has been attributed to the absence of light (as in the
dark phase), low light intensity (as at dawn and dusk), and circadian
rhythm (Kondo et al., 1993). The molecular basis of temporal separation
is not known in any of these cyanobacteria.
The developmentally simple, non-heterocystous cyanobacterium P. boryanum has a versatile physiology that allows it to reversibly modulate uncoupling of the activity of the two photosystems in response
to intracellular nitrogen status (Misra and Tuli, 1993). Under the
experimental conditions of anaerobic bubbling, nitrogenase activity
appeared in a culture of P. boryanum when dissolved oxygen decreased to about 15 µM following the
depression in photosynthetic oxygen evolution (Fig. 1). We earlier
reported that metabolic changes such as changes in the C-N ratio, the
appearance of acetylene reduction activity, and PSII-independent
CO2 fixation (Misra and Tuli, 1993) are
associated with photoautotrophic growth under diazotrophic conditions.
Under such growth conditions, the uncoupling of photosystem activity
(Misra and Tuli, 1994) and impairment of electron transport between
QA and QB (Misra and Desai,
1993) were also linked with the altered excitation energy transfer from phycobilisome to the photosystems (H.S. Misra and S.K. Mahajan, unpublished data).
Cyclic changes in PSII components and nitrogenase activity during
nitrogen fixation growth of P. boryanum were accompanied by
changes in the abundance of the transcripts for several of the relevant
genes. During the N-phase, along with the increase in nifH
transcripts, the multiple-size transcripts that hybridized with
cpcBA, phycocyanin genes, decreased substantially
(Fig. 4). This can result in the disappearance of phycobiliproteins in
the N-phase (Misra and Tuli, 1993) and contribute substantially to the
N-phase-associated impairment of photosynthesis due to inefficient and
altered excitation energy transfer from phycobilisome to the photosystems (results not shown). The down-regulation of
cpcBA in the N-phase agrees with the well-established
disappearance of phycobiliproteins as the first symptom of nitrogen
starvation in both heterocystous and non-heterocystous cyanobacteria
(Stewart, 1980). In Synechocystis sp. strain PCC 6308, the
composition of phycobilisome and its association with soluble and
membrane polypeptides are regulated by the nitrogen status in the cells
(Duke et al., 1989).
Our results suggest that there are at least two copies of
psbA (D1) in P. boryanum, although, as in other
cyanobacteria, their transcripts are not distinguishable by size on
northern blots (Figs. 2 and 4). A low level of expression from the
psbA gene(s) could be due to poor transcription and to rapid
transcript turnover from one or both copies during the N-phase. Such
aspects remained to be examined. However, no specific degradation
product of the psbA transcript was visible during the
N-phase in P. boryanum (Fig. 4), although photosynthetic
electron transport is impaired (Misra and Desai, 1993), leading to
uncoupling of the activity of the two photosystems (Misra and Tuli,
1994). The appearance of a highly stable degradation product of psbA-2
and psbA-3 has been reported in Synechocystis PCC6803 when
photosynthetic electron transport was inhibited (Mohamed et al., 1993).
A differential expression level of psbD (D2) and
psbC (CP43) during temporal separation of photosynthesis in
P. boryanum is particularly interesting. P. boryanum makes two psbD transcripts of 2.8 and 1.6 kb,
which are synthesized constitutively during both the N- and the
P-phases (Fig. 4), while psbC transcripts present in 2.8-kb
mRNA are regulated tightly under diazotrophic conditions. Thus,
P. boryanum may be another exception in which psbC may not be co-transcribed with psbD or may
be regulated differentially. In Anabaena sp. PCC 7120, though psbC is in operon psbD1-C, its transcript
is formed and regulated independently of psbD from an
internal promoter under iron stress (Leonhardt and Straus, 1994). The
constitutive presence of the two psbD transcripts, lack of
hybridization of any of these transcripts with the psbC probe in the N-phase, and the results of Southern hybridization suggest
that P. boryanum may have two copies of psbD,
neither of which is regulated tightly during diazotrophic growth. A
severe decline in the level of transcript for cpcBA,
psbA, and psbC immediately after transfer of the
culture into nitrogen-deficient medium (i.e. N1 in Fig. 3) suggests a
role for these genes in regulating the function of the oxygen-evolving
complex of PSII. A relatively higher level of these transcripts during
the subsequent N-phase (i.e. N2) correlates well with the relatively
higher level of light-dependent oxygen evolution in the N2 compared
with the N1 phase (Fig. 1).
Our study establishes that the accomplishment of alternating cycles of
photosynthesis and dinitrogen fixation in the non-heterocystous cyanobacterium P. boryanum is regulated at the metabolic
level (Rai et al., 1992; Misra and Tuli, 1994) as well as at the
genetic level. The level of transcripts for several genes critical to the function of oxygenic photosynthesis is brought down during microaerobic growth in nitrogen-deficient medium to cause cyclic depression in oxygen evolution even during growth under continuous illumination. Concomitant with the decrease in dissolved oxygen, the
level of the nifH transcripts required for nitrogen fixation rises to allow the fixation of dinitrogen at the expense of carbon reserves built during the preceding photosynthetic phase. The present
study did not attempt to resolve if the cyclic changes in the level of
transcripts were due to regulation of gene expression per se or to
differential stability of a given transcript during the N- and
P-phases. Several interesting questions related to the conversion of
the metabolic signal of N-starvation into a genetic signal that
regulates the level of transcripts central to CO2
and N2 fixation remains to be addressed. P. boryanum provides a promising system with which to study these
aspects, since it is a developmentally simple organism, modulates its
physiology in a highly malleable manner, and can be subjected to
genetic manipulation (Vachhani et al., 1993).
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ACKNOWLEDGMENTS |
We thank Drs. S.K. Mahajan, A.S. Bhagwat, and S.K. Bhattacharji
for technical discussion and critical reading, and R. Haselkorn, A. Grossman, Susan Golden, and C. Jansson for their generous gift of gene probes.
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FOOTNOTES |
Received August 4, 1999; accepted November 4, 1999.
*
Corresponding author; e-mail mbad{at}magnum.barct1.ernet.in;
fax 91-022-5505151.
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