![[Feedback]](/icons/banner/feedbackACT.gif)
![[For Subscribers]](/icons/banner/subscriberACT.gif)
![[Archive]](/icons/banner/archiveACT.gif)
![[Search]](/icons/banner/searchACT.gif)
![[Contents]](/icons/banner/tocACT.gif)
Previous Article | Next Article 
Journal of Bacteriology, December 1998, p. 6392-6395, Vol. 180, No. 23
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Short-Term Regulation of Nitrogenase Activity by
NH4+ in Rhodobacter capsulatus:
Multiple In Vivo Nitrogenase Responses to
NH4+ Addition
Alexander F.
Yakunin and
Patrick C.
Hallenbeck*
Département de Microbiologie et
Immunologie, Université de Montréal, Montréal,
Québec H3C 3J7, Canada
Received 30 July 1998/Accepted 28 September 1998
 |
ABSTRACT |
The photosynthetic bacterium Rhodobacter capsulatus has
been shown to carry out nitrogenase "switch-off," a rapid,
reversible inhibition of in vivo activity. Here, we demonstrate that
highly nitrogen-limited cultures of both the wild-type strain and a
draT draG mutant are capable of nitrogenase switch-off
while moderately nitrogen-limited cultures show instead a
"magnitude" response, with a decrease in in vivo nitrogenase
activity that is proportional to the amount of added
NH4+.
| |
TEXT |
Nitrogenase is an enzymatic complex
consisting of two proteins, MoFe protein (dinitrogenase) and Fe protein
(dinitrogenase reductase), which catalyze the reduction of dinitrogen
to ammonia. Since nitrogen fixation presents significant demands on
cellular energy supplies, many diazotrophs have developed complex
regulatory systems for tight control of nitrogenase synthesis and/or
activity. Several different types of diazotrophs have been shown to be
capable of nitrogenase "switch-off/switch-on," a short-term
(<10-min), reversible modulation of their in vivo activity in response
to various environmental stimuli. In some cases, as amply demonstrated for the photosynthetic bacterium Rhodospirillum rubrum
(13, 15), this response appears to be uniquely mediated by a
two-enzyme system (dinitrogenase reductase ADP-ribosyltransferase
[DRAT] and dinitrogenase reductase-activating glycohydrolase
[DRAG]), which causes a covalent modification/demodification of the
Fe protein via ADP-ribosylation.
Previous studies have shown that the photosynthetic bacterium
Rhodobacter capsulatus is capable of nitrogenase switch-off in response to ammonium additions or darkness (3, 8, 19) and
that the Fe protein from this organism is subject to in vivo (3,
8, 10, 17) and in vitro (4) ADP-ribosylation. Similarly to R. rubrum, R. capsulatus strains
mutated in draT and draG have been reported to be
unable to regulate in vivo nitrogenase activity in response to
NH4+ and darkness (16). However, in
apparent contradiction of these results, it has been reported that this
organism was capable of nitrogenase switch-off in response to ammonium
addition even though the Fe protein had been genetically altered so
that it no longer contained the arginine residue that is the target for
ADP-ribosylation (19). These differences might be explained
by there being another cellular target for DRAT (15).
Alternatively, the previously noted modification-independent regulation
might be subtly altered by growth conditions which have been shown to
affect the switch-off response of some photosynthetic bacteria (1,
24). A full understanding of the differences and commonalities of
these two processes will require extensive biochemical and genetic
analysis. As a prerequisite, we undertook a study of how the switch-off of nitrogenase activity, involving both ADP-ribosylation and
ADP-ribosylation-independent processes, is affected by nitrogen limitation.
The effects of ammonium additions on nitrogenase activity and Fe
protein modification are different depending upon the degree of
nitrogen limitation.
We used cultures of strain SB1003, grown with
different limiting amounts of initial NH4+ (0 to 7.6 mM) in completely filled 1.6- by 12.5-cm screw-capped tubes in a
Biotronette mark III environmental chamber (Labline Instruments)
equipped with three 150-W incandescent bulbs (~3 klx at the tube
surface), for the study of the relationship between in vivo nitrogenase
regulation and Fe protein ADP-ribosylation.
The severity of nitrogen limitation varied with the initial
NH4+ used for growth. Highly nitrogen-limited
(HNL) cultures were grown on RCV medium without an added nitrogen
source. Moderately nitrogen-limited (MNL) cultures were grown on RCV
medium supplemented with 7.6 mM NH4+. HNL
cultures had higher whole-cell glutamine synthetase (GS) activity
(6, 9, 22) and a lower GS adenylylation state (6, 9,
22) than MNL cultures (Table 1). In
the enteric bacteria Salmonella typhimurium and
Klebsiella pneumoniae, the size of the intracellular
glutamine pool appears to reflect the cellular nitrogen status, with
external nitrogen limitation causing a drop in this pool
(5). In agreement with this, quantitation of the levels of
glutamine in R. capsulatus HNL and MNL cultures clearly
showed great differences in the pools of this central nitrogen
metabolite (Table 1).
HNL cultures demonstrated a classical in vivo nitrogenase switch-off
response to added NH4+. Complete inhibition of
acetylene reduction (measured anaerobically at 30°C with 5-ml samples
in 25-ml vials under high light intensity [4]) was
evident within 2 to 3 min of NH4+ addition, and
full recovery of the initial rate of nitrogenase activity was obtained
within a relatively short period of time, which depended upon the
amount of ammonium added (Fig. 1A). To monitor the modification state of Fe protein in R. capsulatus cells under different conditions, a rapid method of
extraction with sodium dodecyl sulfate (SDS), which avoids artifactual
changes in the modification state of Fe protein, was used to directly lyse cells without prior treatment and to solubilize protein for SDS-polyacrylamide gel electrophoresis and subsequent immunoblotting (26). The percentage of unmodified/modified Fe protein
dimers was calculated as ADP-ribosylated Fe protein/total Fe protein (14). Since only one of the two Fe protein subunits in the
Fe protein dimer becomes modified, 100% modification of Fe protein dimers corresponds to two equal-intensity bands. Immunoblot analysis (Fig. 1B and C) showed that the levels of unmodified Fe protein dimers
coincided approximately both temporally and quantitatively with changes
in in vivo nitrogenase activity.
View larger version (16K):
[in this window]
[in a new window]
|
FIG. 1.
Effects of ammonium on in vivo nitrogenase activity
(C2H2 reduction) and the Fe protein
modification state in HNL cultures of R. capsulatus.
Cultures were grown under photoheterotrophic anaerobic conditions on
RCV medium without an added nitrogen source to early stationary phase
(~12 h; extracellular ammonium, ~10 µM; optical density at 660 nm, 1.1; nitrogenase activity, 196 nmol of
C2H4 · min 1 · mg of
protein1), and 5-ml aliquots were transferred by syringe
to 25-ml argon-filled vials for simultaneous analyses of nitrogenase
activity by acetylene reduction and Fe protein modification state by
SDS-polyacrylamide gel electrophoresis and immunoblotting. At the times
indicated by the arrows, NH4Cl was added to a final
concentration of 0.1 mM. (A) In vivo nitrogenase activity
(C2H2 reduction). (B) Immunoblot of Fe protein
in culture samples withdrawn during the C2H2
reduction assay. The lower bands correspond to the monomer form of
unmodified Fe protein, and the upper bands correspond to the
ADP-ribosylated monomer. It should be noted that only one of the two Fe
protein subunits in the Fe protein dimer becomes modified; thus, 100%
modification of Fe protein dimers corresponds to two equal-intensity
bands consisting of an ADP-ribosylated subunit and an unmodified
subunit. (C) Results of scanning densitometry of the immunoblot from
panel B, calculated as percent unmodified Fe protein dimers. Each point
represents an average of at least three replicate assays.
|
|
R. capsulatus cultures grown on RCV medium supplemented with
increasing amounts of ammonium (1.9, 3.8, and 5.7 mM) showed a
progressive decrease in the typical switch-off effect. At an even
higher initial ammonium concentration, 7.6 mM (MNL culture), the
typical switch-off effect was completely lost. At relatively low
concentrations of added ammonium (Fig.
2), only partial inhibition of
nitrogenase activity was observed and there appeared to be no recovery.
Unlike the typical switch-off effects previously observed, where the
quantity of added ammonium affects the duration of the response but not
its magnitude (3, 27), with MNL cultures the quantity of
added ammonium affects the magnitude of the inhibition. These effects
were not due to differences in cell density or light intensity, since
concentration of HNL cultures or dilution of MNL cultures immediately
prior to assay gave essentially the same results as found with
untreated cultures. A similar response has also been observed in the
cyanobacterium Anabaena variabilis (21, 25) and
in the methane-oxidizing bacterium Methylococcus capsulatus (18). This different response, which we term the nitrogenase "magnitude" response, was accompanied by Fe protein
ADP-ribosylation, but the decrease in activity was 1.7-fold greater
than the decrease in unmodified Fe protein (Fig. 2). In these cells,
the modification of Fe protein was not proportional to the added
NH4+ concentration, and similar levels of Fe
protein ADP-ribosylation (25 to 40% modified dimers) were induced by
the addition of 1 or 50 mM NH4+. Thus,
depending on the severity of nitrogen limitation,
NH4+-limited cultures of R. capsulatus demonstrate two different in vivo nitrogenase responses
to NH4+ addition, switch-off and magnitude
responses.
View larger version (21K):
[in this window]
[in a new window]
|
FIG. 2.
Effects of ammonium on in vivo nitrogenase activity
(C2H2 reduction) and the Fe protein
modification state in MNL cultures of R. capsulatus.
Cultures were grown under photoheterotrophic anaerobic conditions on
RCV medium containing 7.6 mM NH4+ as a limiting
nitrogen source to early stationary phase (~16 h; extracellular
ammonium, ~10 µM; optical density at 660 nm, 4.6; nitrogenase
activity, 62 nmol of C2H4 · min1 · mg of protein1). Experimental
details are as described in the legend to Fig. 1. (A) In vivo
nitrogenase activity (C2H2 reduction). (B)
Corresponding immunoblot analysis of Fe protein. (C) Content of
unmodified Fe protein dimers calculated from the scan of the immunoblot
presented in panel B. Each point represents an average of at least
three replicate assays.
|
|
MNL cultures have a decreased level of high-affinity ammonium
transport.
Externally added NH4+ must be
transported into the cell to affect nitrogenase activity, suggesting
that the observed differences might lie at the level of
NH4+ uptake. R. capsulatus possesses
two NH4+ transport systems, a relatively
low-affinity system that appears to be constitutively synthesized and a
high-affinity system that appears to be Ntr regulated (20).
Both HNL and MNL cultures appeared to be metabolically active, as they
showed appreciable rates of NH4+ uptake
(23) (Table 1); this, however, does not differentiate between the two NH4+ transport systems. There
was a marked difference in the two culture types when the high-affinity
system was assayed by using uptake of [14C]methylammonium
(20), with HNL cultures showing a much higher rate (Table
1). Since the total NH4+ transport capabilities
of the two culture types were nearly the same,
NH4+, at the concentrations used here,
presumably enters the cell at the same rate in both HNL and MNL
cultures. However, the difference in activity for the Ntr-regulated
pathway indicates that it is much more active in HNL cultures than in
MNL cultures. Treatments which are thought to inhibit this transport
system, methionine sulfoximine addition (11) or alkaline pH
incubation (12), abolish the switch-off effect (results not
shown). The intracellular concentration of free
NH4+ in nitrogen-fixing cells of
Azotobacter and Rhodobacter spp. is in
the range of 0.2 to 2.6 mM (2, 12). However, the minimal concentration of exogenous NH4+ that can induce
the switch-off response is about 20 to 60 µM (3, 7, 24,
27), suggesting that only extracellular
NH4+ can induce the switch-off response and
therefore that the NH4+ uptake system may play
an important role in the in vivo response of nitrogenase to added
NH4+. Thus, our working hypothesis is that the
switch-off process responds to a signal generated by transport of
NH4+ by the high-affinity system.
Switch-off and magnitude responses are independent of
DRAT and DRAG.
The potential role of the modification
system in the magnitude response was examined with mutant strains that
are incapable of ADP-ribosylation of Fe protein due to inactivation of
the structural genes for DRAT and DRAG (W107I and W107II
[16]). We have found that, similarly to the wild-type
strain, the addition of NH4+ induced a
switch-off response in HNL cultures of these mutants, while the
magnitude response to NH4+ addition was
observed with MNL cultures (Fig. 3 [data
presented only for the W107II mutant]). Western blots confirmed the
absence of ADP-ribosylated Fe protein (results not shown). In these
mutant strains, both nitrogenase responses were less sensitive to
NH4+ since higher NH4+
concentrations were required to induce these responses. Furthermore, incomplete inhibition of in vivo nitrogenase by
NH4+ during the switch-off response was
observed in HNL cultures (Fig. 3). These differences might be directly
due to the absence of in vivo nitrogenase regulation by Fe protein
ADP-ribosylation, or they might be an indirect effect.
View larger version (14K):
[in this window]
[in a new window]
|
FIG. 3.
Effects of ammonium on in vivo nitrogenase activity
(C2H2 reduction) of HNL and MNL cultures of the
R. capsulatus W107II (draT draG) mutant. Cultures
were grown to early stationary phase under photoheterotrophic anaerobic
conditions on RCV medium without an added nitrogen source (A) or
containing 7.6 mM NH4+ as a limiting nitrogen
source (B), as described in the legends to Fig. 1 and 2. (A) HNL
culture. Optical density at 660 nm (OD660), 1.0;
nitrogenase activity, 200 nmol of C2H4 · min1 · mg of protein1; extracellular
ammonium, ~10 µM. (B) MNL culture. OD660, 4.4;
nitrogenase activity, 75 nmol of C2H4 · min1 · mg of protein1; extracellular
ammonium, ~10 µM. Experimental details are as described in the
legend to Fig. 1. Ammonium was added at the times indicated by the
arrows. Each point represents an average of at least three replicate
assays.
|
|
These results indicate that in R. capsulatus,
ADP-ribosylation of either the Fe protein or other cellular components
is not the sole molecular mechanism responsible for in vivo nitrogenase regulation via either the switch-off or the magnitude response. Obviously further investigation is required to determine the molecular mechanisms of the regulation of in vivo nitrogenase activity in R. capsulatus, including determination of the signals for
the various regulatory pathways, the switch-off response
(ADP-ribosylation dependent and/or ADP-ribosylation independent) and
the magnitude response. In this study, we have determined the
experimental conditions necessary for the optimal manifestation and
differentiation of three possible regulatory processes. This should
greatly aid future physiological, biochemical, and genetic dissections
of these different responses.
| |
ACKNOWLEDGMENTS |
This research was supported by grant OGP0036584 from the Natural
Sciences and Engineering Research Council of Canada.
W. Klipp is thanked for generously supplying mutants.
| |
FOOTNOTES |
*
Corresponding author. Mailing address:
Département de Microbiologie et Immunologie,
Université de Montréal, C.P. 6128, succursale Centre-ville,
Montréal, Québec H3C 3J7, Canada. Phone: (514) 343-6278. Fax: (514) 343-5701. E-mail:
patrick.hallenbeck{at}umontreal.ca.
| |
REFERENCES |
| 1.
|
Alef, K.,
D. J. Arp, and W. G. Zumft.
1981.
Nitrogenase switch-off by ammonia in Rhodopseudomonas palustris: loss under nitrogen deficiency and independence from the adenylylation state of glutamine synthetase.
Arch. Microbiol.
130:138-142.
|
| 2.
|
Cordts, M. L., and J. Gibson.
1987.
Ammonium and methylammonium transport in Rhodobacter sphaeroides.
J. Bacteriol.
169:1632-1636[Abstract/Free Full Text].
|
| 3.
|
Hallenbeck, P. C.,
C. M. Meyer, and P. M. Vignais.
1982.
Nitrogenase from the photosynthetic bacterium Rhodopseudomonas capsulata: purification and molecular properties.
J. Bacteriol.
149:708-717[Abstract/Free Full Text].
|
| 4.
|
Hallenbeck, P. C.
1992.
Mutations affecting nitrogenase switch-off in Rhodobacter capsulatus.
Biochim. Biophys. Acta
1118:161-168[Medline].
|
| 5.
|
Ikeda, T. P.,
A. E. Schauger, and S. Kustu.
1996.
Salmonella typhimurium apparently perceives external nitrogen limitation as internal glutamine limitation.
J. Mol. Biol.
259:589-607[Medline].
|
| 6.
|
Johansson, B. C., and H. Gest.
1977.
Adenylylation/deadenylylation control of the glutamine synthetase of Rhodopseudomonas capsulata.
Eur. J. Biochem.
81:365-371[Medline].
|
| 7.
|
Jones, B. L., and K. J. Monty.
1979.
Glutamine as feedback inhibitor of the Rhodopseudomonas sphaeroides nitrogenase system.
J. Bacteriol.
139:1007-1013[Abstract/Free Full Text].
|
| 8.
|
Jouanneau, Y.,
C. M. Meyer, and P. M. Vignais.
1983.
Regulation of nitrogenase activity through iron protein interconversion into an active and inactive form in Rhodopseudomonas capsulata.
Biochim. Biophys. Acta
749:318-328.
|
| 9.
|
Jouanneau, Y.,
S. Lebecque, and P. M. Vignais.
1984.
Ammonia and light effect on nitrogenase activity in nitrogen-limited continuous culture of Rhodopseudomonas capsulata. Role of glutamine synthetase.
Arch. Microbiol.
139:326-331.
|
| 10.
|
Jouanneau, Y.,
C. Roby,
C. M. Meyer, and P. M. Vignais.
1989.
ADP-ribosylation of dinitrogenase reductase in Rhodobacter capsulatus.
Biochemistry
28:6524-6530.
|
| 11.
|
Kleiner, D.,
K. Alef, and A. Hartman.
1983.
Uptake of methionine sulfoximine by some N2 fixing bacteria, and its effect on ammonium transport.
FEBS Lett.
164:121-123[Medline].
|
| 12.
|
Kleiner, D.
1985.
Bacterial ammonium transport.
FEMS Microbiol. Rev.
32:87-100.
|
| 13.
|
Liang, J.,
G. M. Nielsen,
D. P. Lies,
R. H. Burris,
G. P. Roberts, and P. W. Ludden.
1991.
Mutations in the draT and draG genes of Rhodospirillum rubrum result in loss of regulation of nitrogenase by reversible ADP-ribosylation.
J. Bacteriol.
173:6903-6909[Abstract/Free Full Text].
|
| 14.
|
Lowery, R. G.,
L. L. Saari, and P. W. Ludden.
1986.
Reversible regulation of the nitrogenase iron protein from Rhodospirillum rubrum by ADP-ribosylation in vitro.
J. Bacteriol.
166:513-518[Abstract/Free Full Text].
|
| 15.
|
Ludden, P. W., and G. P. Roberts.
1995.
The biochemistry and genetics of nitrogen fixation by photosynthetic bacteria, p. 929-947.
In
R. E. Blankenship, M. T. Madigan, and C. E. Bauer (ed.), Anoxygenic photosynthetic bacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands.
|
| 16.
|
Masepohl, B.,
R. Krey, and W. Klipp.
1993.
The draTG gene region of Rhodobacter capsulatus is required for post-translational regulation of both the molybdenum and the alternative nitrogenase.
J. Gen. Microbiol.
139:2667-2675[Medline].
|
| 17.
|
Michalski, W. P.,
D. J. D. Nicholas, and P. M. Vignais.
1983.
14C-labelling of glutamine synthetase and Fe-protein of nitrogenase in toluene-treated cells of Rhodopseudomonas capsulata.
Biochim. Biophys. Acta
743:136-148.
|
| 18.
|
Murrell, J. C.
1988.
The rapid switch-off of nitrogenase activity in obligate methane-oxidizing bacteria.
Arch. Microbiol.
150:489-495.
|
| 19.
|
Pierrard, J.,
P. W. Ludden, and G. P. Roberts.
1993.
Posttranslational regulation of nitrogenase in Rhodobacter capsulatus: existence of two independent regulatory effects of ammonium.
J. Bacteriol.
175:1358-1366[Abstract/Free Full Text].
|
| 20.
|
Rapp, B. J.,
D. C. Landrum, and J. D. Wall.
1986.
Methylammonium uptake by Rhodobacter capsulatus.
Arch. Microbiol.
146:134-141.
|
| 21.
|
Reich, S.,
H. Almon, and P. Böger.
1986.
Short-term effect of ammonia on nitrogenase activity of Anabaena variabilis (ATCC 29413).
FEMS Microbiol. Lett.
34:53-62.
|
| 22.
|
Shapiro, B. M., and E. R. Stadtman.
1970.
Glutamine synthetase (Escherichia coli).
Methods Enzymol.
17A:910-922.
|
| 23.
|
Solorzano, L.
1969.
Determination of ammonia in natural sea water by the phenolhypochlorite method.
Limnol. Oceanogr.
14:799-801.
|
| 24.
|
Sweet, W. J., and R. H. Burris.
1981.
Inhibition of nitrogenase activity by NH4+ in Rhodospirillum rubrum.
J. Bacteriol.
145:824-831[Abstract/Free Full Text].
|
| 25.
|
Yakunin, A. F.,
O. Y. Troshina,
M. Jha, and I. N. Gogotov.
1992.
Effect of ammonium on nitrogenase activity in the heterocystous cyanobacterium Anabaena variabilis.
Mikrobiologiya
61:256-260.
|
| 26.
|
Yakunin, A. F., and P. C. Hallenbeck.
1998.
A luminol/iodophenol chemiluminescent detection system for Western immunoblots.
Anal. Biochem.
258:146-149[Medline].
|
| 27.
|
Zumft, W. G., and F. Castillo.
1978.
Regulatory properties of the nitrogenase from Rhodopseudomonas palustris.
Arch. Microbiol.
117:53-60[Medline].
|
Journal of Bacteriology, December 1998, p. 6392-6395, Vol. 180, No. 23
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Tremblay, P.-L., Hallenbeck, P. C.
(2008). Ammonia-Induced Formation of an AmtB-GlnK Complex Is Not Sufficient for Nitrogenase Regulation in the Photosynthetic Bacterium Rhodobacter capsulatus. J. Bacteriol.
190: 1588-1594
[Abstract]
[Full Text]
-
Tremblay, P.-L., Drepper, T., Masepohl, B., Hallenbeck, P. C.
(2007). Membrane Sequestration of PII Proteins and Nitrogenase Regulation in the Photosynthetic Bacterium Rhodobacter capsulatus. J. Bacteriol.
189: 5850-5859
[Abstract]
[Full Text]
-
Drepper, T., Gross, S., Yakunin, A. F., Hallenbeck, P. C., Masepohl, B., Klipp, W.
(2003). Role of GlnB and GlnK in ammonium control of both nitrogenase systems in the phototrophic bacterium Rhodobacter capsulatus. Microbiology
149: 2203-2212
[Abstract]
[Full Text]
-
Yakunin, A. F., Hallenbeck, P. C.
(2002). AmtB Is Necessary for NH4+-Induced Nitrogenase Switch-Off and ADP-Ribosylation in Rhodobacter capsulatus. J. Bacteriol.
184: 4081-4088
[Abstract]
[Full Text]
-
Martin, D. E., Reinhold-Hurek, B.
(2002). Distinct Roles of PII-Like Signal Transmitter Proteins and amtB in Regulation of nif Gene Expression, Nitrogenase Activity, and Posttranslational Modification of NifH in Azoarcus sp. Strain BH72. J. Bacteriol.
184: 2251-2259
[Abstract]
[Full Text]
-
Pan, B., Vessey, J. K.
(2001). Response of the Endophytic Diazotroph Gluconacetobacter diazotrophicus on Solid Media to Changes in Atmospheric Partial O2 Pressure. Appl. Environ. Microbiol.
67: 4694-4700
[Abstract]
[Full Text]
-
Egener, T., Martin, D. E., Sarkar, A., Reinhold-Hurek, B.
(2001). Role of a Ferredoxin Gene Cotranscribed with the nifHDK Operon in N2 Fixation and Nitrogenase "Switch-Off" of Azoarcus sp. Strain BH72. J. Bacteriol.
183: 3752-3760
[Abstract]
[Full Text]
-
Arcondeguy, T., Jack, R., Merrick, M.
(2001). PII Signal Transduction Proteins, Pivotal Players in Microbial Nitrogen Control. Microbiol. Mol. Biol. Rev.
65: 80-105
[Abstract]
[Full Text]
-
Jeong, H.-S., Jouanneau, Y.
(2000). Enhanced Nitrogenase Activity in Strains of Rhodobacter capsulatus That Overexpress the rnf Genes. J. Bacteriol.
182: 1208-1214
[Abstract]
[Full Text]
-
Yakunin, A. F., Laurinavichene, T. V., Tsygankov, A. A., Hallenbeck, P. C.
(1999). The Presence of ADP-Ribosylated Fe Protein of Nitrogenase in Rhodobacter capsulatus Is Correlated with Cellular Nitrogen Status. J. Bacteriol.
181: 1994-2000
[Abstract]
[Full Text]
Top
Abstract
Text
