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Regulation of Nitrogen Fixation in Photosynthetic Purple Nonsulfur Bacteria

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Modern Topics in the Phototrophic Prokaryotes

Abstract

Biological nitrogen fixation (BNF) is the nitrogenase-catalyzed process in which dinitrogen (N2) is reduced to ammonia (NH3), the preferred nitrogen source in bacteria. All N2-fixing or diazotrophic bacteria have molybdenum-nitrogenases. In addition, some diazotrophs possess one or two alternative Mo-free nitrogenases, namely a vanadium and/or an iron-only nitrogenase, which are less efficient than Mo-nitrogenase in terms of ATP-consumption per N2 reduced. BNF is widespread in photosynthetic purple nonsulfur bacteria, which are capable of using light energy to generate ATP for nitrogenase activity. This review focusses on BNF regulation in the purple nonsulfur bacteria Rhodobacter capsulatus, Rhodopseudomonas palustris, and Rhodospirillum rubrum. Rp. palustris is one of few diazotrophs having both alternative nitrogenases, whereas Rb. capsulatus and Rs. rubrum have Fe-nitrogenases but no V-nitrogenase. Purple nonsulfur bacteria regulate BNF in response to ammonium, molybdenum, iron, oxygen, and light. BNF regulation involves common regulatory proteins including the two-component nitrogen regulatory system NtrB-NtrC, the transcriptional activator NifA, the nitrogen-specific sigma factor RpoN, the DraT-DraG system for posttranslational nitrogenase regulation, and at least two PII signal transduction proteins. When ammonium is limiting, NtrB phosphorylates NtrC, which in turn activates expression of nifA and other BNF-related genes. NifA and its homologs VnfA and AnfA activate expression of Mo, V, and Fe-nitrogenase genes, respectively, in concert with RpoN. DraT mediates nitrogenase switch-off by ADP-ribosylation upon ammonium addition or light deprivation, the latter condition causing energy depletion. DraG reactivates nitrogenase upon ammonium consumption or reillumination. PII-like proteins integrate the cellular nitrogen, carbon, and energy levels, and control activity of NtrB, NifA, DraT, and DraG. Beside these similarities in BNF regulation, there are species-specific differences. NifA is active as synthesized in Rb. capsulatus, but requires activation by PII in Rp. palustris and Rs. rubrum. Reversible ADP-ribosylation is the only mechanism regulating nitrogenase in Rs. rubrum, whereas Rb. capsulatus and Rp. palustris have additional ADP-ribosylation-independent mechanisms. Last but not least, molybdate directly represses anfA transcription and hence, Fe-nitrogenase expression in Rb. capsulatus, whereas expression of the alternative nitrogenases in Rp. palustris and Rs. rubrum respond to Mo-nitrogenase activity rather than to molybdate directly.

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  1. Lehrstuhl für Biologie der Mikroorganismen, Fakultät für Biologie und Biotechnologie, Ruhr-Universität Bochum, 44780, Bochum, Germany

    Bernd Masepohl

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  1. Department of Biology, Life Sciences Research Center, United States Air Force Academy, Colorado Springs, USA

    Patrick C. Hallenbeck

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Masepohl, B. (2017). Regulation of Nitrogen Fixation in Photosynthetic Purple Nonsulfur Bacteria. In: Hallenbeck, P. (eds) Modern Topics in the Phototrophic Prokaryotes. Springer, Cham. https://doi.org/10.1007/978-3-319-51365-2_1

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