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Article

Regulation of Biological Nitrogen Fixation^{1 ,2}

Department of Biochemistry, University of Wisconsin-Madison, Madison, WI 53706

³To whom correspondence should be addressed.

	ABSTRACT

TOP ABSTRACT INTRODUCTION Properties of nitrogenase. Transcriptional regulation of... Post-translational regulation of... REFERENCES

 
Biological nitrogen fixation, a process found only in some prokaryotes, is catalyzed by the nitrogenase enzyme complex. Bacteria containing nitrogenase occupy an indispensable ecological niche, supplying fixed nitrogen to the global nitrogen cycle. Due to this inceptive role in the nitrogen cycle, diazotrophs are present in virtually all ecosystems, with representatives in environments as varied as aerobic soils (e.g., Azotobacter species), the ocean surface layer (Trichodesmium) and specialized nodules in legume roots (Rhizobium). In any ecosystem, diazotrophs must respond to varied environmental conditions to regulate the tremendously taxing nitrogen fixation process. All characterized diazotrophs regulate nitrogenase at the transcriptional level. A smaller set also possesses a fast-acting post-translational regulation system. Although there is little apparent variation in the sequences and structures of nitrogenases, there appear to be almost as many nitrogenase-regulating schemes as there are nitrogen-fixing species. Herein are described the paradigms of nitrogenase function, transcriptional control and post-translational regulation, as well as the variations on these schemes, described in various nitrogen-fixing bacteria. Regulation is described on a molecular basis, focusing on the functional and structural characteristics of the proteins responsible for control of nitrogen fixation.

KEY WORDS: • nitrogen fixation • nitrogenase • ADP-ribosylation • dinitrogenase reductase ADP-ribosyltransferase • dinitrogenase reductase-activating glycohydrolase

	INTRODUCTION

TOP ABSTRACT INTRODUCTION Properties of nitrogenase. Transcriptional regulation of... Post-translational regulation of... REFERENCES

 
Nitrogen, as an essential dietary element, is derived primarily from animal and plant proteins. The source of biological nitrogen atoms in these proteins can be traced ultimately to nitrogen fixation. Although an increasing proportion of human nutritional nitrogen comes from ammonia fixed by industrial fertilizer production, roughly half of the 23 million metric tons of nitrogen consumed as human food sources (grains and livestock) comes from biological nitrogen fixation by bacteria (1) . Although most bacteria assimilate nitrogen in the form of NH₄⁺ for use in biosynthetic pathways, a more limited set of bacteria is able to convert atmospheric dinitrogen to NH₄⁺. Biological nitrogen fixation is catalyzed by the nitrogenase complex. Nitrogenase catalyzes the conversion of N₂ to NH₄⁺, as represented by: N₂ase

As can be seen by comparison of this reaction to the nitrogen assimilation reactions, nitrogen fixation is very expensive in biological energy equivalents, requiring large amounts of both reducing power and high energy phosphate (ATP). Obligate proton reduction occurs during nitrogenase catalysis, with a minimum of 1 mol of H₂ produced per mol of N₂ reduced (2) . The proportion of electrons allocated to proton reduction increases under conditions of limiting electron flux, further increasing the consumption of MgATP (3) .

In addition to protons, nitrogenase can reduce several other alternative substrates, which resemble N₂ on the basis of double or triple bonds in their structures. Acetylene has proven to be a particularly useful substrate in nitrogenase research because the reduction product, ethylene, is easily quantified by gas chromatography. Because acetylene and ethylene are both permeable to the bacterial envelope, nitrogenase activity may be measured in vivo as well as in vitro by the acetylene reduction method. Reduction of all substrates, except protons, can also be inhibited by CO, suggesting that proton reduction occurs by a slightly different pathway (3) .

	Properties of nitrogenase.

TOP ABSTRACT INTRODUCTION Properties of nitrogenase. Transcriptional regulation of... Post-translational regulation of... REFERENCES

 
A brief description of the properties of nitrogenase proteins is necessary for discussion of their regulation. The nitrogenase complex consists of two metalloproteins, highly conserved in sequence and structure throughout nitrogen-fixing bacteria (4) . The protein containing the site of substrate reduction is nitrogenase molybdenum-iron (MoFe)⁴ protein, also known as dinitrogenase or component I. The obligate electron donor to MoFe protein is nitrogenase iron protein (Fe protein), also known as dinitrogenase reductase or component II. The genes encoding MoFe protein and Fe protein, as well as accessory genes for electron transfer proteins, metal cluster synthesis and regulation comprise the nif regulon (4) .

MoFe protein is a 230-kDa ₂ß₂ tetramer of the nifD and nifK gene products. Each MoFe protein tetramer contains two pairs of metalloclusters unique to MoFe protein, i.e., two molydenum-iron-sulfur-homocitrate clusters (FeMo-co) and two [Fe₈S₇] clusters (P-cluster). FeMo-co consists of two partial cubanes ([Fe₄S₃] and [MoFe₃S₃]) bridged by three sulfides, with homocitrate coordinated to the Mo atom. FeMo-co is completely encompassed by the three domains of the subunit and is the presumed site of substrate reduction (5) . Note that the FeMo-co is structurally distinct from the molybdopterin cofactors found in human oxidase enzymes and nitrate reductase in plants. FeMo-co gives rise to the characteristic electron paramagnetic resonance spectrum of MoFe protein. The P-clusters consist of two distorted iron-sulfur partial cubanes with redox-dependent structure (6) . The P-clusters are located at the interface of the and ß subunits and are thought to be intermediates in the electron transport pathway between Fe protein and FeMo-co (5) .

Fe protein is a 64-kDa ₂ dimer of the nifH gene product. A single, regular [Fe₄S₄] cubane is symmetrically coordinated between the subunits by Cys97 and Cys132 from each subunit. This [Fe₄S₄] cluster is the redox-active center directly involved with electron transfer to MoFe protein. The [Fe₄S₄] cluster of Fe protein cycles between the reduced (1+) state and the oxidized (2+) state during electron transfer to MoFe protein. An all-ferrous (0) state of Fe protein has also been described (7) , but the physiologic relevance of this species is unclear. Each Fe protein dimer can bind two nucleotide molecules, at sites distal from the [Fe₄S₄] active site (3) . Binding of MgATP at these sites causes a conformational change in Fe protein. The two subunits rotate toward each other, extruding the [Fe₄S₄] cluster toward the protein surface (and surmised interaction with the P-clusters of MoFe protein) by 4 Å (8) . This conformational change is thought to be a key step in the catalytic cycle of nitrogenase.

Using data obtained from the nitrogenase systems of Clostridium pasteurianum, Klebsiella pneumoniae and Azotobacter vinelandii, a general sequence of events in the catalytic cycle of nitrogenase can be described. MgATP binding to reduced Fe protein shifts the redox potential of the [Fe₄S₄]^2+/1+ couple from about -300 mV to nearly -450 mV vs. standard hydrogen electrode. A concomitant MgATP-induced conformational change apparently promotes interaction of Fe protein with MoFe protein (3) . Upon complex formation, an additional conformational change of Fe protein shifts the redox potential of the Fe₄S₄ cluster by an additional -200 mV (9) , making the transfer of a single electron from the Fe protein to MoFe protein energetically favorable. The hydrolysis of MgATP (bound to Fe protein) to MgADP and P_i is coupled to this electron transfer. After electron transfer and MgATP hydrolysis, the nitrogenase complex dissociates in the rate-limiting step of the cycle. Fe protein is then reduced by a low potential electron donor (a ferredoxin or flavodoxin in vivo), and MgADP is exchanged for MgATP. The catalytic cycle is repeated until a sufficient number of electrons have been transferred to completely reduce the FeMo-cobound substrate (3) . Although Fe protein is the obligate electron donor for MoFe protein in all characterized nitrogenase systems, the in vivo electron donor for Fe protein is less stringently conserved. The NifJ NifF Fe protein electron donation pathway, described in K. pneumoniae (10) , is replaced with a number of electron donors in other species, particularly ferredoxins of varying FeS cluster composition.

	Transcriptional regulation of nitrogenase.

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Nitrogen fixation is regulated at the transcriptional level in response to environmental oxygen and ammonium levels. Because the nitrogenase components are oxygen labile, it is advantageous for bacteria to repress transcription when oxygen levels are high. It is also advantageous to repress the expression of the metabolically expensive nitrogenase system when the cellular level of fixed nitrogen is sufficiently high. The degree to which each stimulus affects transcription is characteristic of the particular diazotroph. Expression of nitrogenase in symbiotic diazotrophs is fairly insensitive to ammonium because export of ammonium to their symbiont suppresses ammonium levels. The expression of nif genes in free-living diazotrophs is more sensitive to cellular ammonium levels (11) .

As with the nitrogen assimilation and the nitrogenase mechanisms, the paradigm of transcriptional regulation is derived from studies on K. pneumoniae. In this model, control of nif gene expression focuses on NifA (the nifA gene product), a ⁵⁴ (rpoN gene product)-dependent transcriptional activator, responsible for control of all major nif gene cluster transcription. Transcription of nifA is under the control of the ntrBC gene products, which comprise a global two-component transcriptional activator system, responsible for cellular nitrogen regulation (11) . In the paradigm system, K. pneumoniae, the nifA gene is cotranscribed with nifL, which encodes a redox- and nitrogen-responsive regulatory flavoprotein (NifL). NifL acts as a negative regulator of NifA, effectively adding another level of regulation in response to oxygen and fixed nitrogen. Oxidized NifL is also sensitive to the presence of nucleotides in vitro, with increased inhibition especially in response to ADP (12) . The means by which NifL inhibits NifA remain to be determined.

Deviations from the K. pneumoniae paradigm exist in nearly all nitrogen fixation organisms of research interest (Fig. 1 ). In A. vinelandii (11) and Rhodospirillum rubrum (Y. Zhang, unpublished results), expression of nifA is not under the control of the ntrBC gene products, and it remains unclear whether nifA expression is under nitrogen control. In Rhizobium meliloti, redox-dependent control of nifA expression occurs in response to fixL and fixJ, which encode a two-component regulatory system responsive to oxygen (11) . This system apparently replaces the ntrBC control found in K. pneumoniae. R. meliloti also lacks NifL, but NifA still appears to be inhibited by oxygen stimulus (13) . Similarly, there is no evidence for NifL in Rhodobacter capsulatus. R. capsulatus contains nif-related genes analogous to ntrBC, but the expression of an rpoN-like gene is found to be sensitive to oxygen and fixed nitrogen status (11) . Also, R. capsulatus contains two copies of nifA, which respond differently to ammonium (14) . Clearly, nitrogenase transcriptional control mechanisms must be elucidated separately for any given diazotroph.

View larger version (21K): [in this window] [in a new window]   Figure 1. Comparative models of transcriptional regulation of nif genes in (A) Klebsiella pneumoniae, (B) Rhizobium meliloti, (C) Rhodospirillum rubrum and (D) Rhodobacter capsulatus. PII (the glnB gene product) and GlnK are global nitrogen regulation proteins of similar structure. RpoN is the 54 subunit of the RNA polymerase complex. Functionally similar regulatory proteins are symbolized identically in each panel. Solid and dashed lines indicate positive and negative regulation, respectively. Solid circles indicate promoter sites. R. meliloti model adapted from (27) .

	Post-translational regulation of nitrogenase.

TOP ABSTRACT INTRODUCTION Properties of nitrogenase. Transcriptional regulation of... Post-translational regulation of... REFERENCES

View larger version (26K): [in this window] [in a new window]   Figure 2. Model of in vivo nitrogenase Fe protein regulation in Rhodospirillum rubrum by reversible ADP-ribosylation. Small molecules required for dinitrogenase reductase ADP-ribosyltransferase (DRAT) and dinitrogenase reductase-activating glycohydrolase (DRAG) activities in vitro are shown beside the enzyme symbols. Adapted from (19) .

The genes encoding DRAT (draT) and DRAG (draG) are cotranscribed from a non-nif operon, which includes a third gene (draB) of unknown function. The configuration of the draTGB operon is conserved in A. brasilense (Y. Zhang, unpublished results) and A. lipoferum (17) . R. capsulatus, however, lacks draB (18) . DRAT acts as a 30-kDa monomer with high specificity toward oxidized, MgADP-bound Fe protein, possessing no measurable activity with other arginine residues or water as the ADP-ribose acceptor (15 ,19) . The amino acid sequence of DRAT is not highly similar to those of the bacterial toxins, but the structural domains are expected to be similar and some key residues are conserved. Surprisingly, the Fe proteins from K. pneumoniae and A. vinelandii (which lack the dra operon) are better substrates for R. rubrum DRAT than the R. rubrum Fe protein itself. There are no measurable reverse or glycohydrolytic reactions catalyzed by DRAT. The removal of the ADP-ribose group is instead catalyzed by dinitrogenase reductase-activating glycohydrolase (DRAG), which restores fully active Fe protein with an intact Arg101 side chain. DRAG is a 32-kDa monomeric binuclear manganese enzyme that is capable of cleaving the -N-glycosidic bond of a number of analogs of ADP-ribosylarginine (15) . However, only the reduced, MgATP-bound form (not the MgADP-bound or nucleotide-free forms) of ADP-ribosylated Fe protein is a substrate for DRAG (15 ,19) . Although the exact modes of interaction of DRAT and DRAG with Fe protein are unknown, it is believed that each binds the same surface of Fe protein as does MoFe protein, as evidenced by the inhibition of cellular nitrogenase activity by overexpressed DRAT (20) .

Although the means by which DRAT and DRAG are each regulated are not well understood, it is known that the activity of each enzyme is regulated in vivo (21 ,22) . Because the in vivo activation and inactivation rates are reflected by in vitro assay rates using purified components, it is believed that the regulatory signals involve either negative effectors or known assay components. As noted above, DRAT and DRAG have opposite specificities for MgADP- and MgATP-bound Fe protein. However, cellular fluctuations in ATP and ADP levels during inactivation/activation cycles are insufficient to account for the dramatic nitrogenase activity regulation (15) . The recently demonstrated sensitivity of DRAT and DRAG toward the redox state of Fe protein suggests the possibility that DRAT and DRAG may be regulated by sensing the cellular energy and redox status directly from the state of Fe protein (19) . The cellular NAD⁺ concentration has also been suggested as a possible positive effector for DRAT (23) . Apparently, unregulated variants of DRAG have altered divalent cation affinities (K. Kim, unpublished results), suggesting a potential means of regulation by weak, reversible binding of Fe²⁺ or Mn²⁺ ion in DRAG.

Although the nitrogenase-inactivating conditions of nitrogen sufficiency (NH₄⁺) and energy limitation (darkness) give rise to convergent signal transduction pathways, it remains unclear where the pathways converge. Inhibition of glutamine synthetase perturbs both responses, suggesting an intermediary role for glutamine (21) . However, the cellular concentration of glutamine is relatively unaffected by the modification and demodification of Fe protein (24) . Also, genetic perturbations of nitrogen control genes (glnB, ntrBC) yield results that do not support the model of closely related signal transduction pathways because the effects on ammonia response appear to be independent of the darkness response (25, Y. Zhang, unpublished results) .

The response of DRAT and DRAG activities to exogenous inactivation effectors is not species specific. Plasmid-borne draTG genes from A. brasilense restored the wild-type phenotype to dra mutants of R. rubrum (26) , so that Fe protein was inactivated in response to darkness, but not anaerobicity. Transformants of K. pneumoniae carrying a plasmid containing draTGB from R. rubrum have been shown to reversibly ADP-ribosylate Fe protein in response to exogenous ammonium (C. Halbleib, unpublished results). Thus, DRAT and DRAG appear to sense a global regulatory signal, present even in nitrogen-fixing bacteria that lack the dra operon.

The multiple layers and redundant mechanisms of nitrogenase regulation attest to the biological necessity of proper control of biological nitrogen fixation (27) . Future research in the nitrogen fixation field will be required to clarify the regulatory mechanisms not only in the paradigm systems, but also in those organisms (e.g., legume-associated microbes) whose contributions to the global nitrogen cycle are most critical.

	FOOTNOTES

 
¹ Supported by National Institute of General Medical Science grant #GM54910 and National Institutes of Health grant #5 T32 GM08349.

² Manuscript received 11 February 2000. Initial review completed 23 February 2000.

⁴ Abbreviations used: DRAG, dinitrogenase reductase-activating glycohydrolase; DRAT, dinitrogenase reductase ADP-ribosyltransferase; FeMo-co, iron-molybdenum cofactor; Fe protein, nitrogenase iron protein; MoFe protein, nitrogenase molybdenum-iron protein.

	REFERENCES

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