J Bacteriol, April 1998, p. 1965-1969, Vol. 180, No. 7
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Evidence for a Regulatory Link of Nitrogen Fixation
and Photosynthesis in Rhodobacter capsulatus via
HvrA
Monika
Kern,
Paul-Bertram
Kamp,
Annette
Paschen,
Bernd
Masepohl, and
Werner
Klipp*
Ruhr-Universität Bochum, Fakultät
für Biologie, Lehrstuhl für Biologie der
Mikroorganismen, D-44780 Bochum, Germany
Received 14 October 1997/Accepted 27 January 1998
 |
ABSTRACT |
A Rhodobacter capsulatus reporter strain, carrying a
constitutively expressed nifA gene and a
nifH-lacZ gene fusion, was used for random transposon
Tn5 mutagenesis to search for genes required for the
NtrC-independent ammonium repression of NifA activity. A mutation in
hvrA, which is known to be involved in low-light activation
of the photosynthetic apparatus, released both ammonium and oxygen
control of nifH expression in this reporter strain, demonstrating a regulatory link of nitrogen fixation and photosynthesis via HvrA. In addition, a significant increase in
bacteriochlorophyll a (BChla) content was found
in cells under nitrogen-fixing conditions. HvrA was not involved in
this up-regulation of BChla. Instead, the presence of
active nitrogenase seemed to be sufficient for this process,
since no increase in BChla content was observed in
different nif mutants.
| |
TEXT |
Under anaerobic conditions in the
light, the phototrophic purple bacterium Rhodobacter
capsulatus is able to fix atmospheric dinitrogen. A large number
of genes involved in synthesis and regulation of the molybdenum
nitrogenase and the alternative, heterometal-free nitrogenase have been
identified and characterized in detail (for a review, see reference
21). Both nitrogenase systems are only expressed
under conditions of ammonium depletion, and a regulatory cascade
resembling the general nitrogen regulation (ntr) system of enteric bacteria has been proposed for
R. capsulatus (8, 13, 19, 20). Homologs of NtrB
(NifR2), NtrC (NifR1), and GlnB (NifR5) are responsible for
sensing and responding to the intracellular concentration of fixed
nitrogen. Under nitrogen limitation the phosphorylated form of NtrC
activates the transcription of a number of genes, including
nifA1/nifA2 and anfA, which encode the
transcriptional activators of the molybdenum and the
alternative nitrogenase, respectively. However, in contrast to all
known members of the NtrC family, R. capsulatus NtrC does
not activate its target genes in concert with the RNA polymerase
containing 
54 (9-11, 13, 19). The R. capsulatus rpoN (nifR4) gene encoding 54
is part of the nitrogen fixation regulon and forms an autoregulatory circuit activated by NifA and AnfA, respectively (5, 21). These transcriptional activators in turn stimulate the expression of
all other nitrogen fixation genes in a 54-dependent
manner. However, nitrogen fixation in R. capsulatus is not
only regulated at the transcriptional level but also at the
posttranslational level. In response to ammonium and darkness, the
draTG gene products control the activity of dinitrogenase reductase of both nitrogenase systems by reversible, covalent ADP-ribosylation (23).
In addition, the NifA-dependent transcriptional activation is
negatively regulated at the posttranslational level by ammonium in an
NtrC-independent manner (12). In Klebsiella
pneumoniae and Azotobacter vinelandii, an additional
regulatory protein, NifL, is responsible for modulation of NifA
activity in response to oxygen and fixed nitrogen. However, there is no
evidence for a nifL-like gene in R. capsulatus
(for a review, see reference 21). In addition, the
domain structure of R. capsulatus NifA differs from NifA of
K. pneumoniae and A. vinelandii (22)
and corresponds to the rhizobial type of oxygen-sensitive NifA proteins (for a review, see reference 7), which in general
seem to be independent of regulation by NifL homologs.
In phototrophic bacteria the high energy demand of the nitrogen
fixation process can be fulfilled by photosynthesis. Genes encoding the
reaction center, the light-harvesting complex and proteins involved in
synthesis of the corresponding pigments, are only expressed under
anaerobic conditions. In addition, synthesis of the photosynthetic
apparatus is regulated by light intensity (for a review, see reference
1). Regulatory genes involved in this dual control
are clustered in one region of the chromosome and include a
two-component regulatory system (regA-regB) responsible for
oxygen regulation (15, 26-28) and two genes
(hvrA and hvrB) necessary for low-light
activation (2, 3). Recently, the regA-regB
systems in Rhodospirillum rubrum and Rhodobacter
sphaeroides were shown not only to regulate photosystem
biosynthesis and transcription of genes required for CO2
fixation but also to control the ability of these bacteria to grow
under nitrogen-fixing conditions (15).
In this paper we present evidence that HvrA, which was previously shown
to be responsible for light regulation of the photosynthetic apparatus,
is also involved in the NtrC-independent ammonium control of
nif gene expression. The observed increase of the
bacteriochlorophyll a (BChla) content under
conditions of nitrogen fixation further corroborates the hypothesis of
a regulatory link of photosynthesis and nitrogen fixation.
Identification of an R. capsulatus gene
(hvrA) involved in NtrC-independent ammonium regulation of
nif gene expression.
Contrary to earlier models of
nif gene regulation, constitutive expression of
nifA1 did not result in ammonium-independent expression of a nifH-lacZ reporter gene fusion in
R. capsulatus (12). This repression by high
ammonium concentrations was not affected by mutations in
ntrC or glnB (12). However,
constitutively expressed nifA genes from K. pneumoniae and Rhizobium meliloti complemented an
R. capsulatus nifA1 nifA2 double mutant, but neither of the
heterologous nifA gene products was affected by ammonium, indicating that the ammonium sensitivity is a specific property of
R. capsulatus NifA (21).
To identify genes involved in ammonium repression of NifA activity, we
performed a random transposon Tn5 mutagenesis
(18) of R. capsulatus W49I/R372I (a derivative of
R. capsulatus B10S [18]) carrying a
constitutively expressed nifA1 gene
[nifA1(Con)] and a chromosomally integrated
nifH-lacZYA reporter gene fusion (12).
Tn5-induced mutants (kanamycin resistant) were screened for
the ability to form deep blue colonies in the presence of ammonium on
solid RCV medium supplemented with X-Gal
(5-bromo-4-chloro-3-indolyl-
-D-galactopyranoside) under
anaerobic phototrophic growth conditions. Expression of the
nifH-lacZ fusion in mutant strains identified by this
procedure was quantified by measuring -galactosidase activity of
cells grown in liquid RCV medium containing either ammonium or serine as nitrogen source. Among 70,000 kanamycin-resistant mutants, three
strains (M3-4, M7-1, and M8-20) were identified, which showed significant expression of the nifH-lacZ fusion in the
presence of ammonium (Table 1).
Tn5-containing EcoRI fragments from these mutant
strains were cloned and analyzed by DNA sequencing. Tn5
insertions in mutant strains M7-1 and M8-20 mapped within the
nifH promoter region at distances of 52 and 55 bp upstream
of the nifH start codon, respectively. It seemed reasonable
that insertion of Tn5 at these positions created promoters
constitutively expressing the nifH-lacZ fusion. In general,
Tn5 insertions result in polar mutations, but nonpolar
Tn5 insertions have also been described for the
nifR3-R2-R1 (nifR3-ntrBC) gene region
(14). Since promoter sequences are not yet well defined in
R. capsulatus, these artificial promoters created by fusion
of Tn5 and target sequences in the nifH promoter region were not obvious from the DNA sequence.
As shown in Fig. 1, the Tn5
insertion in M3-4 was localized within the hvrA gene, which
is part of a regulatory gene cluster involved in the oxygen and light
regulation of the photosynthetic apparatus (3). To ensure
that the phenotype observed in M3-4 did not result from a secondary
mutation, we reconstructed the hvrA mutation in the
background of the parental strain W49I/R372I. For this purpose, mutant
strains M3-47, M3-42I, and M3-42II were constructed (Fig. 1). For the
construction of M3-47, the Tn5-containing EcoRI
fragment from mutant M3-4 was first cloned into the mobilizable plasmid
pWKR102A (4) prior to replacement of the
Tn5-internal 3.4-kb HindIII fragment by a
2-kb HindIII fragment carrying a 
-Km cassette. The
resulting hybrid plasmid was introduced into the parental strain
W49I/R372I, and marker rescue resulted in M3-47, carrying the -Km
cassette at the original site of Tn5 insertion. Mutant
strains M3-42I and M3-42II, carrying a deletion encompassing the 3' end
of hvrA, the hvrB gene, and part of Orf5, were
constructed in a similar manner. Mutants M3-42I and M3-42II are
distinguished by the orientation of the Km resistance gene. Correct
homogenotization of interposons was verified in each case by Southern
hybridization (data not shown). As found for the original Tn5 mutant, the reconstructed interposon mutant strains
M3-47, M3-42I, and M3-42II formed deep blue colonies on X-Gal plates in
the presence of ammonium (data not shown), corroborating the conclusion
that the mutation of hvrA indeed was responsible for the
observed phenotype.
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FIG. 1.
Organization of regulatory photosynthesis genes in
R. capsulatus and localization of mutations affecting
NifA-dependent expression of nif genes. The physical
and genetic organization of the photosynthesis gene cluster has been
described previously (2, 3). Heavy lines indicate the DNA
fragments sequenced in this study. The position of Tn5
insertion in mutant M3-4 [nifA(Con) nifH-lacZ
hvrA::Tn5] is marked by a vertical
arrow. Numbers in parentheses correspond to the hvrA
sequence determined by Buggy et al. (3). Locations of a
hvrA interposon insertion (M3-47) and two deletions
encompassing hvrA, hvrB, and Orf5 (M3-42I and
M3-42II) are indicated. The sizes of the interposon cassettes are not
drawn to scale.
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Disruption of hvrA leads to nifH expression
in the presence of ammonium and oxygen.
For a more detailed study
of the ammonium regulation of nifH-lacZ expression in mutant
strains M3-47, M3-42I, and M3-42II, in comparison to the parental
strain W49I/R372I [nifA(Con) nifH-lacZYA], all
strains were grown phototrophically in the presence of either ammonium or serine as nitrogen source under anaerobic conditions. In
contrast to the parental strain, which showed little nifH
expression in the presence of ammonium, the mutants strongly expressed
the nifH-lacZ fusion under these conditions (Fig.
2A), and the levels of -galactosidase
activities were in the range of the maximum activity obtained with the
parental strain under nitrogenase-derepressing conditions (serine as
nitrogen source [22]). Moreover, in the presence of
serine, the mutant strains showed about two times greater
-galactosidase activities than the parental strain.
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FIG. 2.
Influence of hvrA mutations on NifA-dependent
expression of nifH-lacZ. Mutant strains M3-42I, M3-42II, and
M3-47 contain the hvrA insertion or deletion mutations
outlined in the legend to Fig. 1, respectively, in the background of
the parental strain W49I/R372I [nifA1(Con)
nifH-lacZYA]. -Galactosidase activities expressed in mU
per mg of protein (nmoles of o-nitrophenol × min 1 × mg of protein1) were determined as
described previously (6). (A) Cells were grown under
phototrophic conditions in the presence of ammonium (7.5 mM) or serine
(9.5 mM) as nitrogen source. Data shown are means of at least three
independent experiments measured as triplicates, and the standard error
in each case was less than 20%. (B) Cells were grown either
aerobically or microaerobically (for details, see text) with serine
(9.5 mM) as the nitrogen source. -Galactosidase activities shown are
the averages of two independent experiments measured as triplicates.
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|
Since R. capsulatus NifA belongs to the class of interdomain
linker-containing NifA proteins, which were shown to be regulated by
oxygen (7), the effect of hvrA mutations on this
regulation was studied (Fig. 2B). All strains were cultivated in RCV
medium containing serine under either aerobic or microaerobic
conditions. Aerobic growth was achieved by growing 20-ml cultures in
500-ml flasks with shaking (150 rpm). For growth under microaerobic
conditions, 70-ml cultures were incubated in 100-ml flasks with shaking
(150 rpm). After aerobic or microaerobic growth only negligible
-galactosidase activities were detected for the parental strain
W49I/R372I. In contrast, all mutant strains expressed the
nifH-lacZ fusion in the presence of oxygen. No significant
differences in the level of -galactosidase activities could be
observed between high- and low-oxygen cultures (Fig. 2B), whereas
strictly anaerobic conditions resulted in a further, about 40-fold
increase of nifH expression (Fig. 2A).
No significant differences in ammonium or oxygen control between the
hvrA insertion mutant M3-47 and the
hvrA-hvrB-Orf5 deletion mutants M3-42I and M3-42II were
obvious, indicating that neither hvrB nor Orf5 contributed
to the observed phenotype. In conclusion, HvrA is not only involved in
low-light activation of the photosynthetic apparatus (3) but
also influences the modulation of NifA activity by oxygen and ammonium.
Induction of active nitrogenase is paralleled by an increase in
pigment synthesis.
To fulfill the high energy demand imposed by
nitrogen fixation, photosynthetic bacteria can use photosynthesis to
create ATP and low potential redox equivalents. This energetic
link between photosynthesis and nitrogen fixation was reflected by a
significantly increased pigment content found in nitrogen-fixing
cultures of R. capsulatus wild type B10S compared to
ammonium-grown cells (Fig. 3A). In
contrast, mutant strain M3-47 [nifA(Con)
nifH-lacZ hvrA::-Km] lacked the
ability to increase photopigment synthesis under
nitrogenase-derepressing conditions (Fig. 3B).
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FIG. 3.
Spectral analysis of photopigments of R. capsulatus wild-type B10S (A) and mutant strain M3-47 (B). M3-47
contains the hvrA mutation outlined in the legend to Fig. 1
in the background of strain W49I/R372I [nifA(Con)
nifH-lacZYA]. Cells were grown for 48 h to late
exponential phase (optical density at 660 nm, 1.0) under
nitrogenase-repressing (15 mM ammonium, solid lines) or -derepressing
(9.5 mM serine, hatched lines) high-light conditions (approximately
10,000 lx). BChla was extracted from equal amounts of cells,
and spectral analysis was carried out as described previously
(16).
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To determine whether the observed differences in phenotypes were a
consequence of hvrA disruption or constitutive expression of
nifA or were due to lack of an active, energy-consuming
nitrogenase, we measured BChla content and nitrogenase
activities of mutant strains affected in each of the corresponding
genes (Table 2). Neither a single
hvrA mutation (B10S-47) nor a constitutively expressed
nifA gene (W49I) affected the increase of BChla
content under nitrogenase-derepressing conditions compared to
nitrogen-replete conditions. In contrast, R. capsulatus
R372I carrying a chromosomal nifH-lacZ fusion showed no
increase in BChla content. Since the integration of the
nifH-lacZ fusion into the chromosome abolished the
expression of nifHDK and thus prevents synthesis of
nitrogenase apoproteins, it was tempting to assume that the lack of
active nitrogenase was the major reason for the observed phenotype. To test this hypothesis, strains carrying lesions in nifR1 and
nifR4 encoding NtrC and 54, two major
regulatory components necessary for nif gene expression, were analyzed. In addition, a nifQ mutant strain, which is
able to synthesize active nitrogenase only in the presence of 1 mM Na2MoO4 (25), was tested. As shown
in Table 2, the ability to synthesize active nitrogenase was directly
paralleled with the increase of BChla content, whereas HvrA
did not influence this regulation. These results indicated that the
high demand for ATP and/or redox equivalents of nitrogenase, which are
necessary to reduce nitrogen to ammonia, are involved in the
up-regulation of the photosynthetic apparatus.
It is worth noting that the hvrA mutant strain B10S-47
exhibited an increased specific nitrogenase activity compared to the wild type (Table 2). This would be in line with the finding that nifH expression was also significantly increased under
nitrogenase-derepressing conditions in hvrA mutant strains
(Fig. 2). These results indicate that HvrA might directly or indirectly
act as a general negative effector of the nitrogen fixation process.
Conclusions.
Disruption of the hvrA gene allowed
NifA-dependent nif gene expression in the presence of
ammonium and oxygen, but an hvrA mutation did not affect
photosynthetic growth or nitrogenase activity under the high-light
conditions used in this study. Therefore, it is unlikely that the
observed phenotype was due to altered transport of ammonium or to a
reduced photosynthetic capacity resulting in an altered energy charge
of the cells. One might speculate that HvrA modulates the activity of a
not yet identified signal-transducing cascade involved in the
posttranslational regulation of NifA. Since HvrA belongs to the class
of histone-like, DNA-binding proteins, it seems more likely that HvrA
either affects binding of NifA to its upstream activator sequence or
influences DNA bending between the upstream activator sequence and the
54-RNA polymerase binding site. However, since it is
known that histone-like proteins are involved in the regulation of a
large number of genes in other bacterial species, it could not be
excluded that indirect effects are responsible for the observed
phenotypes.
| |
ACKNOWLEDGMENTS |
This work was supported by financial grants from the Deutsche
Forschungsgemeinschaft, Fonds der Chemischen Industrie, and Bundesministerium für Forschung und Technologie.
| |
FOOTNOTES |
*
Corresponding author. Mailing address:
Ruhr-Universität Bochum, Fakultät für Biologie,
Lehrstuhl für Biologie der Mikroorganismen, D-44780 Bochum,
Germany. Phone: 49-(0)234-700-3100. Fax: 49-(0)234-7094-620. E-mail:
werner.klipp{at}ruhr-uni-bochum.de.
Present address: Klinische Kooperationseinheit für
Dermato-Onkologie am Klinikum Mannheim,
Theodor-Kutzerufer 1, D-68135 Mannheim, Germany.
| |
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J Bacteriol, April 1998, p. 1965-1969, Vol. 180, No. 7
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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