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Dissection of the Bradyrhizobium japonicum NifA+σ54 regulon, and identification of a ferredoxin gene (fdxN) for symbiotic nitrogen fixation

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Abstract

Hierarchically organized regulatory proteins form a complex network for expression control of symbiotic and accessory genes in the nitrogen-fixing soybean symbiont Bradyrhizobium japonicum. A genome-wide survey of regulatory interactions was made possible with the design of a custom-made gene chip. Here, we report the first use of the microarray in a comprehensive and complete characterization of the B. japonicum NifA+σ54 regulon which forms an important node in the entire network. Comparative transcript profiles of anaerobically grown wild-type, nifA, and rpoN 1/2 mutant cells were complemented with a position-specific frequency matrix-based search for NifA- and σ54-binding sites plus a simple operon definition. One of the newly identified NifA+σ54-dependent genes, fdxN, encodes a ferredoxin required for efficient symbiotic nitrogen fixation, which makes it a candidate for being a direct electron donor to nitrogenase. The fdxN gene has an unconventional, albeit functional σ54 promoter with the dinucleotide GA instead of the consensus GC motif at position −12. A GC-containing mutant promoter and the atypical GA-containing promoter of the wild type were disparately activated. Expression analyses were also carried out with two other NifA+σ54 targets (ectC; ahpC). Incidentally, the tiling-like design of the microarray has helped to arrive at completely revised annotations of the ectC- and ahpC-upstream DNA regions, which are now compatible with promoter locations. Taken together, the approaches used here led to a substantial expansion of the NifA+σ54 regulon size, culminating in a total of 65 genes for nitrogen fixation and diverse other processes.

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References

  • Alexeyev MF (1995) Three kanamycin resistance gene cassettes with different polylinkers. Biotechniques 18:52–54

    PubMed  CAS  Google Scholar 

  • Alvarez-Morales A, Hennecke H (1985) Expression of Rhizobium japonicum nifH and nifDK operons can be activated by the Klebsiella pneumoniae NifA protein but not by the product of NtrC. Mol Gen Genet 199:306–314

    Article  PubMed  CAS  Google Scholar 

  • Alvarez-Morales A, Betancourt-Alvarez M, Kaluza K, Hennecke H (1986) Activation of the Bradyrhizobium japonicum nifH and nifDK operons is dependent on promoter-upstream DNA sequences. Nucleic Acids Res 14:4207–4227

    Article  PubMed  CAS  Google Scholar 

  • Ampe F, Kiss E, Sabourdy F, Batut J (2003) Transcriptome analysis of Sinorhizobium meliloti during symbiosis. Genome Biol 4:R15

    Article  PubMed  Google Scholar 

  • Babst M, Hennecke H, Fischer HM (1996) Two different mechanisms are involved in the heat-shock regulation of chaperonin gene expression in Bradyrhizobium japonicum. Mol Microbiol 19:827–839

    Article  PubMed  CAS  Google Scholar 

  • Barnett MJ, Toman CJ, Fisher RF, Long SR (2004) A dual-genome symbiosis chip for coordinate study of signal exchange and development in a prokaryote-host interaction. Proc Natl Acad Sci USA 101:16636–16641

    Article  PubMed  CAS  Google Scholar 

  • Barrios H, Grande R, Olvera L, Morett E (1998) In vivo genomic footprinting analysis reveals that the complex Bradyrhizobium japonicum fixRnifA promoter region is differently occupied by two distinct RNA polymerase holoenzymes. Proc Natl Acad Sci USA 95:1014–1019

    Article  PubMed  CAS  Google Scholar 

  • Bauer CC, Scappino L, Haselkorn R (1993) Growth of the cyanobacterium Anabaena on molecular nitrogen: NifJ is required when iron is limited. Proc Natl Acad Sci USA 90:8812–8816

    Article  PubMed  CAS  Google Scholar 

  • Bauer E, Kaspar T, Fischer HM, Hennecke H (1998) Expression of the fixR-nifA operon in Bradyrhizobium japonicum depends on a new response regulator, RegR. J Bacteriol 180:3853–3863

    PubMed  CAS  Google Scholar 

  • Bebbington KJ, Williams HD (2001) A role for DNA supercoiling in the regulation of the cytochrome bd oxidase of Escherichia coli. Microbiology 147:591–598

    PubMed  CAS  Google Scholar 

  • Becker A, Berges H, Krol E, Bruand C, Rüberg S, Capela D, Lauber E, Meilhoc E, Ampe F, de Bruijn FJ, Fourment J, Francez-Charlot A, Kahn D, Kuster H, Liebe C, Pühler A, Weidner S, Batut J (2004) Global changes in gene expression in Sinorhizobium meliloti 1021 under microoxic and symbiotic conditions. Mol Plant Microbe Interact 17:292–303

    Article  PubMed  CAS  Google Scholar 

  • Belitsky BR, Sonenshein AL (1999) An enhancer element located downstream of the major glutamate dehydrogenase gene of Bacillus subtilis. Proc Natl Acad Sci USA 96:10290–10295

    Article  PubMed  CAS  Google Scholar 

  • Benos PV, Bulyk ML, Stormo GD (2002) Additivity in protein-DNA interactions: how good an approximation is it? Nucleic Acids Res 30:4442–4451

    Article  PubMed  CAS  Google Scholar 

  • Bernstein JA, Khodursky AB, Lin PH, Lin-Chao S, Cohen SN (2002) Global analysis of mRNA decay and abundance in Escherichia coli at single-gene resolution using two-color fluorescent DNA microarrays. Proc Natl Acad Sci USA 99:9697–9702

    Article  PubMed  CAS  Google Scholar 

  • Black LK, Maier RJ (1995) IHF-dependent and RpoN-dependent regulation of hydrogenase expression in Bradyrhizobium japonicum. Mol Microbiol 16:405–413

    Article  PubMed  CAS  Google Scholar 

  • Bobik C, Meilhoc E, Batut J (2006) FixJ: a major regulator of the oxygen limitation response and late symbiotic functions of Sinorhizobium meliloti. J Bacteriol 188:4890–4902

    Article  PubMed  CAS  Google Scholar 

  • Buchanan-Wollaston V, Cannon MC, Beynon JL, Cannon FC (1981) Role of the nifA gene product in the regulation of nif expression in Klebsiella pneumoniae. Nature 294:776–778

    Article  PubMed  CAS  Google Scholar 

  • Buck M, Khan H, Dixon R (1985) Site-directed mutagenesis of the Klebsiella pneumoniae nifL and nifH promoters and in vivo analysis of promoter activity. Nucleic Acids Res 13:7621–7638

    Article  PubMed  CAS  Google Scholar 

  • Buck M, Cannon W, Woodcock J (1987) Transcriptional activation of the Klebsiella pneumoniae nitrogenase promoter may involve DNA loop formation. Mol Microbiol 1:243–249

    Article  PubMed  CAS  Google Scholar 

  • Caldelari Baumberger I, Fraefel N, Göttfert M, Hennecke H (2003) New NodW- or NifA-regulated Bradyrhizobium japonicum genes. Mol Plant Microbe Interact 16:342–351

    Article  PubMed  Google Scholar 

  • Capela D, Filipe C, Bobik C, Batut J, Bruand C (2006) Sinorhizobium meliloti differentiation during symbiosis with alfalfa: a transcriptomic dissection. Mol Plant Microbe Interact 19:363–372

    Article  PubMed  CAS  Google Scholar 

  • Carlson TA, Martin GB, Chelm BK (1987) Differential transcription of the two glutamine synthetase genes of Bradyrhizobium japonicum. J Bacteriol 169:5861–5866

    PubMed  CAS  Google Scholar 

  • Carter KR, Rawlings J, Orme-Johnson WH, Becker RR, Evans HJ (1980) Purification and characterization of a ferredoxin from Rhizobium japonicum bacteroids. J Biol Chem 255:4213–4223

    PubMed  CAS  Google Scholar 

  • Casadaban MJ, Martinezarias A, Shapira SK, Chou J (1983) β-galactosidase gene fusions for analyzing gene expression in Escherichia coli and yeast. Methods Enzymol 100:293–308

    Article  PubMed  CAS  Google Scholar 

  • Chun JY, Stacey G (1994) A Bradyrhizobium japonicum gene essential for nodulation competitiveness is differentially regulated from two promoters. Mol Plant Microbe Interact 7:248–255

    PubMed  CAS  Google Scholar 

  • Chun JY, Sexton GL, Roth LE, Stacey G (1994) Identification and characterization of a novel Bradyrhizobium japonicum gene involved in host-specific nitrogen fixation. J Bacteriol 176:6717–6729

    PubMed  CAS  Google Scholar 

  • Crooks GE, Hon G, Chandonia J-M, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190

    Article  PubMed  CAS  Google Scholar 

  • Dainese-Hatt P, Fischer HM, Hennecke H, James P (1999) Classifying symbiotic proteins from Bradyrhizobium japonicum into functional groups by proteome analysis of altered gene expression levels. Electrophoresis 20:3514–3520

    Article  PubMed  CAS  Google Scholar 

  • Daniel RM, Appleby CA (1972) Anaerobic-nitrate, symbiotic and aerobic growth of Rhizobium japonicum: effects on cytochrome P450, other haemoproteins, nitrate and nitrite reductases. Biochim Biophys Acta 275:347–354

    Article  PubMed  CAS  Google Scholar 

  • Dixon R, Kahn D (2004) Genetic regulation of biological nitrogen fixation. Nature reviews. Microbiology 2:621–631

    PubMed  CAS  Google Scholar 

  • Dixon RA, Henderson NC, Austin S (1988) DNA supercoiling and aerobic regulation of transcription from the Klebsiella pneumoniae nifLA promoter. Nucleic Acids Res 16:9933–9946

    Article  PubMed  CAS  Google Scholar 

  • Ebeling S, Noti JD, Hennecke H (1987) Mapping and nucleotide sequence of the nifS promoter of Bradyrhizobium japonicum. Nucleic Acids Res 15:9598

    Article  PubMed  CAS  Google Scholar 

  • Ebeling S, Noti JD, Hennecke H (1988) Identification of a new Bradyrhizobium japonicum gene (frxA) encoding a ferredoxin like protein. J Bacteriol 170:1999–2001

    PubMed  CAS  Google Scholar 

  • Edgren T, Nordlund S (2005) Electron transport to nitrogenase in Rhodospirillum rubrum: identification of a new fdxN gene encoding the primary electron donor to nitrogenase. FEMS Microbiol Lett 245:345–351

    Article  PubMed  CAS  Google Scholar 

  • Edgren T, Nordlund S (2006) Two pathways of electron transport to nitrogenase in Rhodospirillum rubrum: the major pathway is dependent on the fix gene products. FEMS Microbiol Lett 260:30–35

    Article  PubMed  CAS  Google Scholar 

  • Elsen S, Swem LR, Swem DL, Bauer CE (2004) RegB/RegA, a highly conserved redox-responding global two-component regulatory system. Microbiol Mol Biol Rev 68:263–279

    Article  PubMed  CAS  Google Scholar 

  • Fischer HM (1994) Genetic regulation of nitrogen fixation in rhizobia. Microbiol Rev 58:352–386

    PubMed  CAS  Google Scholar 

  • Fischer HM, Hennecke H (1987) Direct response of Bradyrhizobium japonicum nifA-mediated nif gene regulation to cellular oxygen status. Mol Gen Genet 209:621–626

    Article  PubMed  CAS  Google Scholar 

  • Fischer HM, Alvarez-Morales A, Hennecke H (1986) The pleiotropic nature of symbiotic regulatory mutants: Bradyrhizobium japonicum nifA gene is involved in control of nif gene expression and formation of determinate symbiosis. EMBO J 5:1165–1173

    PubMed  CAS  Google Scholar 

  • Fischer HM, Babst M, Kaspar T, Acuña G, Arigoni F, Hennecke H (1993) One member of a groESL-like chaperonin multigene family in Bradyrhizobium japonicum is coregulated with symbiotic nitrogen-fixation genes. EMBO J 12:2901–2912

    PubMed  CAS  Google Scholar 

  • Fuhrmann M, Hennecke H (1984) Rhizobium japonicum nitrogenase Fe protein gene (nifH). J Bacteriol 158:1005–1011

    PubMed  CAS  Google Scholar 

  • Gonnet GH, Hallett MT, Korostensky C, Bernardin L (2000) Darwin v. 2.0: an interpreted computer language for the biosciences. Bioinformatics 16:101–103

    Article  PubMed  CAS  Google Scholar 

  • Göttfert M, Hitz S, Hennecke H (1990) Identification of nodS and nodU, two inducible genes inserted between the Bradyrhizobium japonicum nodYABC and nodIJ genes. Mol Plant Microbe Interact 3:308–316

    PubMed  Google Scholar 

  • Göttfert M, Röthlisberger S, Kündig C, Beck C, Marty R, Hennecke H (2001) Potential symbiosis-specific genes uncovered by sequencing a 410-kilobase DNA region of the Bradyrhizobium japonicum chromosome. J Bacteriol 183:1405–1412

    Article  PubMed  Google Scholar 

  • Gubler M (1989) Fine-tuning of nif and fix gene expression by upstream activator sequences in Bradyrhizobium japonicum. Mol Microbiol 3:149–159

    Article  PubMed  CAS  Google Scholar 

  • Gubler M, Hennecke H (1988) Regulation of the fixA gene and fixBC operon in Bradyrhizobium japonicum. J Bacteriol 170:1205–1214

    PubMed  CAS  Google Scholar 

  • Gubler M, Zürcher T, Hennecke H (1989) The Bradyrhizobium japonicum fixBCX operon: identification of fixX and of a 5′ mRNA region affecting the level of the fixBCX transcript. Mol Microbiol 3:141–148

    Article  PubMed  CAS  Google Scholar 

  • Hahn M, Hennecke H (1984) Localized mutagenesis in Rhizobium japonicum. Mol Gen Genet 193:46–52

    Article  CAS  Google Scholar 

  • Hauser F, Lindemann A, Vuilleumier S, Patrignani A, Schlapbach R, Fischer HM, Hennecke H (2006) Design and validation of a partial-genome microarray for transcriptional profiling of the Bradyrhizobium japonicum symbiotic gene region. Mol Genet Genomics 275:55–67

    Article  PubMed  CAS  Google Scholar 

  • Herrgard MJ, Covert MW, Palsson BO (2004) Reconstruction of microbial transcriptional regulatory networks. Curr Opin Biotechnol 15:70–77

    Article  PubMed  CAS  Google Scholar 

  • Hoover TR, Santero E, Porter S, Kustu S (1990) The integration host factor stimulates interaction of RNA polymerase with NifA, the transcriptional activator for nitrogen fixation operons. Cell 63:11–22

    Article  PubMed  CAS  Google Scholar 

  • Johansson M, Nordlund S (1996) Transcription of the glnB and glnA genes in the photosynthetic bacterium Rhodospirillum rubrum. Microbiology 142:1265–1272

    PubMed  CAS  Google Scholar 

  • Jouanneau Y, Meyer C, Naud I, Klipp W (1995) Characterization of an fdxN mutant of Rhodobacter capsulatus indicates that ferredoxin I serves as electron donor to nitrogenase. Biochim Biophys Acta 1232:33–42

    Article  PubMed  Google Scholar 

  • Kaluza K, Hennecke H (1984) Fine structure analysis of the nifDK operon encoding the α and β subunits of dinitrogenase from Rhizobium japonicum. Mol Gen Genet 196:35–42

    Article  CAS  Google Scholar 

  • Kaneko T, Nakamura Y, Sato S, Minamisawa K, Uchiumi T, Sasamoto S, Watanabe A, Idesawa K, Iriguchi M, Kawashima K, Kohara M, Matsumoto M, Shimpo S, Tsuruoka H, Wada T, Yamada M, Tabata S (2002) Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 9:189–197

    Article  PubMed  Google Scholar 

  • Klipp W, Reiländer H, Schlüter A, Krey R, Pühler A (1989) The Rhizobium meliloti fdxN gene encoding a ferredoxin-like protein is necessary for nitrogen fixation and is cotranscribed with nifA and nifB. Mol Gen Genet 216:293–302

    Article  PubMed  CAS  Google Scholar 

  • Kullik I, Fritsche S, Knobel H, Sanjuan J, Hennecke H, Fischer HM (1991) Bradyrhizobium japonicum has two differentially regulated, functional homologs of the σ54 gene (rpoN). J Bacteriol 173:1125–1138

    PubMed  CAS  Google Scholar 

  • Kuzma MM, Hunt S, Layzell DB (1993) Role of oxygen in the limitation and inhibition of nitrogenase activity and respiration rate in individual soybean nodules. Plant Physiol 101:161–169

    PubMed  CAS  Google Scholar 

  • Lawrence CE, Altschul SF, Boguski MS, Liu JS, Neuwald AF, Wootton JC (1993) Detecting subtle sequence signals—a Gibbs sampling strategy for multiple alignment. Science 262:208–214

    Article  PubMed  CAS  Google Scholar 

  • Liu X, De Wulf P (2004) Probing the ArcA-P modulon of Escherichia coli by whole genome transcriptional analysis and sequence recognition profiling. J Biol Chem 279:12588–12597

    Article  PubMed  CAS  Google Scholar 

  • Liu YJ, Hu B, Zhu JB, Shen SJ, Yu GQ (2005) nifH promoter activity is regulated by DNA supercoiling in Sinorhizobium meliloti. Acta Biochim Biophys Sin (Shanghai) 37:221–226

    Article  CAS  Google Scholar 

  • Martin GB, Thomashow MF, Chelm BK (1989) Bradyrhizobium japonicum glnB, a putative nitrogen-regulatory gene, is regulated by NtrC at tandem promoters. J Bacteriol 171:5638–5645

    PubMed  CAS  Google Scholar 

  • Merrick MJ, Coppard JR (1989) Mutations in genes downstream of the rpoN gene (encoding σ54) of Klebsiella pneumoniae affect expression from σ54-dependent promoters. Mol Microbiol 3:1765–1775

    Article  PubMed  CAS  Google Scholar 

  • Mesa S, Bedmar EJ, Chanfon A, Hennecke H, Fischer HM (2003) Bradyrhizobium japonicum NnrR, a denitrification regulator, expands the FixLJ–FixK2 regulatory cascade. J Bacteriol 185:3978–3982

    Article  PubMed  CAS  Google Scholar 

  • Mockler TC, Chan S, Sundaresan A, Chen H, Jacobsen SE, Ecker JR (2005) Applications of DNA tiling arrays for whole-genome analysis. Genomics 85:1–15

    Article  PubMed  CAS  Google Scholar 

  • Mulder NJ, Apweiler R, Attwood TK, Bairoch A, Bateman A, Binns D, Bork P, Buillard V, Cerutti L, Copley R, Courcelle E, Das U, Daugherty L, Dibley M, Finn R, Fleischmann W, Gough J, Haft D, Hulo N, Hunter S, Kahn D, Kanapin A, Kejariwal A, Labarga A, Langendijk-Genevaux PS, Lonsdale D, Lopez R, Letunic I, Madera M, Maslen J, McAnulla C, McDowall J, Mistry J, Mitchell A, Nikolskaya AN, Orchard S, Orengo C, Petryszak R, Selengut JD, Sigrist CJ, Thomas PD, Valentin F, Wilson D, Wu CH, Yeats C (2007) New developments in the InterPro database. Nucleic Acids Res 35:D224–D228

    Article  PubMed  CAS  Google Scholar 

  • Munch R, Hiller K, Grote A, Scheer M, Klein J, Schobert M, Jahn D (2005) Virtual footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Bioinformatics 21:4187–4189

    Article  PubMed  CAS  Google Scholar 

  • Mwangi M, Siggia E (2003) Genome wide identification of regulatory motifs in Bacillus subtilis. BMC Bioinformatics 4:18

    Article  PubMed  Google Scholar 

  • Nellen-Anthamatten D, Rossi P, Preisig O, Kullik I, Babst M, Fischer HM, Hennecke H (1998) Bradyrhizobium japonicum FixK2, a crucial distributor in the FixLJ-dependent regulatory cascade for control of genes inducible by low oxygen levels. J Bacteriol 180:5251–5255

    PubMed  CAS  Google Scholar 

  • Nienaber A, Huber A, Göttfert M, Hennecke H, Fischer HM (2000) Three new NifA-regulated genes in the Bradyrhizobium japonicum symbiotic gene region discovered by competitive DNA-RNA hybridization. J Bacteriol 182:1472–1480

    Article  PubMed  CAS  Google Scholar 

  • Norrander J, Kempe T, Messing J (1983) Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene 26:101–106

    Article  PubMed  CAS  Google Scholar 

  • Noti JD, Folkerts O, Turken AN, Szalay AA (1986) Organization and characterization of genes essential for symbiotic nitrogen fixation from Bradyrhizobium japonicum I110. J Bacteriol 167:774–783

    PubMed  CAS  Google Scholar 

  • Prell J, Poole P (2006) Metabolic changes of rhizobia in legume nodules. Trends Microbiol 14:161–168

    Article  PubMed  CAS  Google Scholar 

  • Regensburger B, Hennecke H (1983) RNA polymerase from Rhizobium japonicum. Arch Microbiol 135:103–109

    Article  PubMed  CAS  Google Scholar 

  • Roberts M (2005) Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst 1:5

    Article  PubMed  CAS  Google Scholar 

  • Roelvink PW, Harmsen M, van Kammen A, van den Bos RC (1990) The nifH promoter region of Rhizobium leguminosarum: nucleotide sequence and promoter elements controlling activation by NifA protein. Gene 87:31–36

    Article  PubMed  CAS  Google Scholar 

  • Samanta MP, Tongprasit W, Istrail S, Cameron RA, Tu Q, Davidson EH, Stolc V (2006) The transcriptome of the sea urchin embryo. Science 314:960–962

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russel DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Sciotti MA, Chanfon A, Hennecke H, Fischer HM (2003) Disparate oxygen responsiveness of two regulatory cascades that control expression of symbiotic genes in Bradyrhizobium japonicum. J Bacteriol 185:5639–5642

    Article  PubMed  CAS  Google Scholar 

  • Scott KF, Rolfe BG, Shine J (1983) Biological nitrogen fixation: primary structure of the Rhizobium trifolii iron protein gene. DNA 2:149–155

    Article  PubMed  CAS  Google Scholar 

  • Shah VK, Stacey G, Brill WJ (1983) Electron transport to nitrogenase. Purification and characterization of pyruvate:flavodoxin oxidoreductase, the nifJ gene product. J Biol Chem 258:12064–12068

    PubMed  CAS  Google Scholar 

  • Simon R, Priefer U, Pühler A (1983) Vector plasmids for in vivo and in vitro manipulation of gram-negative bacteria. In: Pühler A (ed) Molecular genetics of the bacteria–plant interaction. Springer, Heidelberg, pp 98–106

    Google Scholar 

  • Studholme DJ, Dixon R (2003) Domain architectures of σ54-dependent transcriptional activators. J Bacteriol 185:1757–1767

    Article  PubMed  CAS  Google Scholar 

  • Uchiumi T, Ohwada T, Itakura M, Mitsui H, Nukui N, Dawadi P, Kaneko T, Tabata S, Yokoyama T, Tejima K, Saeki K, Omori H, Hayashi M, Maekawa T, Sriprang R, Murooka Y, Tajima S, Simomura K, Nomura M, Suzuki A, Shimoda Y, Sioya K, Abe M, Minamisawa K (2004) Expression islands clustered on the symbiosis island of the Mesorhizobium loti genome. J Bacteriol 186:2439–2448

    Article  PubMed  CAS  Google Scholar 

  • Valderrama B, Davalos A, Girard L, Morett E, Mora J (1996) Regulatory proteins and cis-acting elements involved in the transcriptional control of Rhizobium etli reiterated nifH genes. J Bacteriol 178:3119–3126

    PubMed  CAS  Google Scholar 

  • Weidenhaupt M, Fischer HM, Acuña G, Sanjuan J, Hennecke H (1993) Use of a promoter-probe vector system in the cloning of a new NifA-dependent promoter (ndp) from Bradyrhizobium japonicum. Gene 129:33–40

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Andrea Patrignani, Ralph Schlapbach, Ulrich Wagner from the Functional Genomics Center Zürich (FGCZ) are greatly acknowledged for their contribution to the microarray experiments. We thank Jürg Hauser for programming assistance in the tiling array analysis. Financial support for this work was provided by the Swiss National Foundation for Scientific Research and the ETH through Research Programs for the FGCZ.

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  1. Institute of Microbiology, Eidgenössische Technische Hochschule, Wolfgang-Pauli-Strasse 10, 8093, Zürich, Switzerland

    Felix Hauser, Gabriella Pessi, Christoph Weber, Nicola Rusca, Andrea Lindemann, Hans-Martin Fischer & Hauke Hennecke

  2. Institute of Computational Science, Eidgenössische Technische Hochschule, Universitätsstrasse 6, 8092, Zürich, Switzerland

    Markus Friberg

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  1. Felix Hauser
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Hauser, F., Pessi, G., Friberg, M. et al. Dissection of the Bradyrhizobium japonicum NifA+σ54 regulon, and identification of a ferredoxin gene (fdxN) for symbiotic nitrogen fixation. Mol Genet Genomics 278, 255–271 (2007). https://doi.org/10.1007/s00438-007-0246-9

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