Biological nitrogen fixation has an important role in the nitrogen cycle and provides a substantial input of fixed nitrogen into soils. It is widely distributed amongst the Bacteria and Archaea but is not found in eukaryotes. Nitrogen-fixing bacteria are found in a wide variety of habitats including both soil and marine environments and in symbiotic associations with termites, ferns, woody plants and legumes.
Nitrogenase, the enzyme that catalyses biological nitrogen fixation, is oxygen sensitive and requires ATP and an electron donor for activity. The enzyme consists of two metalloprotein components — the Fe protein and the MoFe protein — which contain different metal clusters. Electron transfer from the Fe protein to the MoFe protein is ATP-dependent and each step in nitrogen reduction involves an obligatory cycle of association and dissociation of the component proteins. The oxygen sensitivity of nitrogenase and the energetic requirements for nitrogen fixation impose physiological constraints on diazotrophs, necessitating tight regulation of nitrogen fixation (nif) genes in response to the levels of fixed nitrogen, carbon, energy and the external oxygen concentration.
Common regulatory components and similar regulatory networks are used to control nitrogen fixation, but there is considerably plasticity in the regulatory networks, which differ from species to species, dependent on host physiology. In the Proteobacteria, most nif genes are activated by the enhancer-binding protein NifA together with the RNA polymerase sigma factor σ54. The expression of NifA and, in many cases its activity, is controlled by regulatory cascades that are responsive to different environmental cues.
Four proteins regulate nitrogen fixation in response to oxygen or redox signals. In symbiotic bacteria, FixL (a haemoprotein sensor histidine kinase) and NifA provide a hierarchical response to the oxygen concentration. In other diazotrophs, NifA is not directly responsive to oxygen but its activity is regulated by a partner flavoprotein, NifL, that senses the redox status. The histidine protein kinase RegB and its homologues respond to redox through an active cysteine and might sense the electron flux through a high affinity cbb3-type oxidase.
The nitrogen status is communicated to target regulatory proteins by the PII signal-transduction proteins that are covalently modified by uridylylation under nitrogen-limiting conditions. Many bacteria contain more than one homologue of PII, enabling hierarchical regulation in response to the level of fixed nitrogen. In free-living diazotrophic bacteria that have the NifL–NifA regulatory system, the PII-like protein GlnK regulates NifA activity by completely different mechanisms, illustrating the plasticity of protein–protein interactions in these systems.
Some bacteria have the remarkable capacity to fix atmospheric nitrogen to ammonia under ambient conditions, a reaction only mimicked on an industrial scale by a chemical process that requires high temperatures, elevated pressure and special catalysts. The ability of microorganisms to use nitrogen gas as the sole nitrogen source and engage in symbioses with host plants confers many ecological advantages, but also incurs physiological penalties because the process is oxygen sensitive and energy dependent. Consequently, biological nitrogen fixation is highly regulated at the transcriptional level by sophisticated regulatory networks that respond to multiple environmental cues.
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Work in the laboratory of R.D. is supported by the UK Biotechnology and Biosciences Research Council. Work in the laboratory of D.K. is supported by the Centre National de la Recherche Scientifique and the Institut National de la Recherche Agronomique. We thank Michael Chan for the kind gift of images for use in Figure 4. We thank many of our colleagues for helpful discussions and apologise for the multitude of work in this field which is not cited in this article due to space constraints. This review is dedicated to Werner Klipp, who sadly passed away in 2002 and made many contributions to research on gene regulation in nitrogen-fixing bacteria.
The authors declare no competing financial interests.
The Protein Data Bank
- DIAZOTROPHIC ORGANISMS
A nitrogen-fixing organism that is capable of growth on atmospheric nitrogen as the sole nitrogen source.
An organism that is capable of using CO, CO2 or carbonates as the sole source of carbon for cell biosynthesis and that derives energy from the oxidation of reduced inorganic compounds.
Symbiotic associations of plants that have the capacity to form root nodules with nitrogen-fixing actinomycetes.
- TRANSITION-STATE ANALOGUE
A substrate designed to mimic the properties or the geometry of the transition state of a reaction. This is an intermediate state in which the enzyme has reached a geometric and energetic state necessary to overcome the activation energy required for the reaction.
A plant protein that is specifically found, or strongly induced, in root nodules.
A differentiated intracellular form of a rhizobial cell, specialized in nitrogen fixation.
- NITROGEN FIXATION GENES
These are found in both free-living and symbiotic nitrogen-fixing bacteria. They include the structural genes for nitrogenase, genes that are required for nitrogenase biosynthesis and regulatory genes.
Upstream activator sequences that provide specific recognition sequences for the NifA protein in the vicinity of σ54 -dependent nif promoters.
A domain that was named after three proteins that contain it: cGMP-stimulated phosphodiesterases, Anabaena adenyl cyclase and Escherichia coli FhlA.
Describes the step in which the DNA sequence in the RNA polymerase–promoter complex is unwound.
A subunit from which a larger protein structure is built.
- FIX GENES
Genes in addition to nif genes that are required for nitrogen fixation in symbiotic bacteria. Homologues of some of the fix genes are also present in bacteria that do not fix nitrogen.
A condition in which oxygen is present at subsaturating concentrations.
This domain was named after three eukaryotic proteins — PER, ARNT and SIM — in which it is found. In these proteins, the domain detects signals through an associated cofactor.
- SURFACE PLASMON RESONANCE
An optical phenomenon that occurs when light is reflected by thin metal films. The technology is used to monitor the progress of biomolecular interactions (for example, protein–protein interactions) in real-time.
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Dixon, R., Kahn, D. Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2, 621–631 (2004). https://doi.org/10.1038/nrmicro954
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