Skip to main content
SpringerLink
Log in

Nitrogen fixation control in Herbaspirillum seropedicae

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Herbaspirillum seropedicae is a Gram-negative endophytic diazotroph that associates with important agricultural crops. Several studies have shown that this organism can contribute to plant growth suggesting potential for use as a biofertilizer. Nitrogen fixation in H. seropedicae is highly regulated both at the transcriptional and post-translational levels. Both of these regulatory levels respond to the ammonium availability in the external medium through a cascade of interacting proteins. The transcriptional regulation of the process also responds to oxygen, which is probably directly sensed by the transcriptional regulator NifA. Here, we review current knowledge of the regulation of nitrogen fixation in H. seropedicae. The signal transduction protein GlnK is a key regulator of nitrogen fixation at both the transcriptional and post-translational levels. In vitro analysis indicates that GlnK interacts with NifA and probably modulates its activity, thereby controlling nif expression. GlnK, together with the ammonium channel protein AmtB, also participates in the post-translational regulation of nitrogenase activity by an unidentified mechanism. This regulatory system efficiently controls nitrogen fixation according to prevailing fixed nitrogen and oxygen levels in H. seropedicae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Araújo LM, Monteiro RA, Souza EM, Steffens MB, Rigo LU, Pedrosa FO, Chubatsu LS (2004) GlnB is specifically required for Azospirillum brasilense NifA activity in Escherichia coli. Res Microbiol 155:491–495

    Article  PubMed  Google Scholar 

  • Arcondéguy T, van Heeswijk W, Merrick M (1999) Studies on the roles of GlnK and GlnB in regulating Klebsiella pneumoniae NifL dependent control. FEMS Microbiol Lett 180:263–270

    Article  PubMed  Google Scholar 

  • Arcondéguy T, Jack R, Merrick M (2001) P(II) signal transduction proteins, pivotal players in microbial nitrogen control. Microbiol Mol Biol Rev 65:80–105

    Article  PubMed  Google Scholar 

  • Arsene F, Kaminski PA, Elmerich C (1999) Control of Azospirillum brasilense NifA activity by PII: effect of replacing Tyr residues of the NifA N-terminal domain on NifA activity. FEMS Microbiol Lett 179:339–343

    Article  PubMed  CAS  Google Scholar 

  • Baldani JI, Baldani VLD, Seldin L, Dobereiner J (1986) Characterization of Herbaspirillum seropedicae gen. nov., sp. nov., a root-associated nitrogen-fixing bacterium. Int J Syst Bacteriol 36:86–93

    Article  CAS  Google Scholar 

  • Baldani VLD, Baldani JI, Olivares F, Dobereiner J (1992) Identification and ecology of Herbaspirillum seropedicae and the closely related Pseudomonas rubrisubalbicans. Symbiosis 13:65–73

    Google Scholar 

  • Baldani JI, Pot B, Kirchhof G, Falsen E, Baldani VLD, Olivares FL, Hoste B, Kersters K, Hartmann A, Gillis M, Dobereiner J (1996) Emended description of Herbaspirillum; inclusion of [Pseudomonas] rubrisubalbicans, a milk plant pathogen, as Herbaspirillum rubrisubalbicans com. nov.; and classification of a group of clinical isolates (EF group 1) as Herbaspirillum species 3. Int J Syst Bacteriol 46:802–810

    Article  PubMed  CAS  Google Scholar 

  • Benelli EM, Souza EM, Funayama S, Rigo LU, Pedrosa FO (1997) Evidence for two possible glnB-type genes in Herbaspirillum seropedicae. J Bacteriol 179:4623–4626

    PubMed  CAS  Google Scholar 

  • Benelli EM, Buck M, Souza EM, Yates MG, Pedrosa FO (2001) Uridylylation of the PII protein from Herbaspirillum seropedicae. Can J Microbiol 47:309–314

    PubMed  CAS  Google Scholar 

  • Benelli EM, Buck M, Polikarpov I, Souza EM, Cruz LM, Pedrosa FO (2002) Herbaspirillum seropedicae signal transduction protein PII is structurally similar to the enteric GlnK. Eur J Biochem 269:3296–3303

    Article  CAS  Google Scholar 

  • Bonatto AC, Souza EM, Pedrosa FO, Yates MG, Benelli EM (2005) Effect of T- and C- loop mutations on the Herbaspirillum seropedicae GlnB protein in nitrogen signalling. Res Microbiol 156:634–640

    Article  PubMed  CAS  Google Scholar 

  • Bonatto AC, Couto GH, Souza EM, Araújo LM, Pedrosa FO, Noindorf L, Benelli EM (2007) Purification and characterization of bifunctional uridylyltransferase and the signal transducing proteins GlnB and GlnK from H. seropedicae. Protein Expr Purif 55:293–299

    Article  PubMed  CAS  Google Scholar 

  • Brigle KE, Weiss MC, Newton WE, Dean DR (1987) Products of the iron-molybdenum cofactor-specific biosynthetic genes, nifE and nifN, are structurally homologous to the products of the nitrogenase molybdenum-iron protein genes, nifD and nifK. J Bacteriol 169:1547–1553

    PubMed  CAS  Google Scholar 

  • Bulen WA, Lecomte JR (1966) The nitrogenase system of Azotobacter: two- enzyme requirement for N2 reduction, ATP-dependent H2 evolution, and ATP hydrolysis. Proc Natl Acad Sci USA 56:979–986

    Article  PubMed  CAS  Google Scholar 

  • Carr PD, Cheah E, Suffolk PM, Vasudevan SG, Dixon NE, Ollis DL (1996) X-ray structure of the signal transduction protein from Escherichia coli at 1.9 A. Acta Crystallog D Biol Crystallog 52:93–104

    Article  CAS  Google Scholar 

  • Chen S, Liu L, Zhou X, Elmerich C, Li J (2005) Functional analysis of the GAF domain of NifA in Azospirillum brasilense: Effects of Tyr→Phe mutations on NifA and its interaction with GlnB. Mol Gen Genomics 273:415–422

    Article  CAS  Google Scholar 

  • Ding L, Yokota A (2004) Proposals of Curvibacter gracilis gen. nov., sp. nov. and Herbaspirillum putei sp. nov. for bacterial strains isolated from well water and reclassification of [Pseudomonas] huttiensis, [Pseudomonas] lanceolata, [Aquaspirillum] delicatum and [Aquaspirillum] autotrophicum as Herbaspirillum huttiense comb. nov., Curvibacter lanceolatus comb. nov., Curvibacter delicatus comb. nov. and Herbaspirillum autotrophicum comb. nov. Int J Syst Envol Microbiol 54:2223–2230

    Article  CAS  Google Scholar 

  • Dixon R, Kahn D (2004) Genetic Regulation of biological nitrogen fixation. Nat Rev Microbiol 2:621–631

    Article  PubMed  CAS  Google Scholar 

  • Dobritsa AP, Reddy MC, Samadpour M (2010) Reclassification of Herbaspirillum putei as a later heterotypic synonym of Herbaspirillum huttiense, with description of H. huttiense subsp. huttiense subsp. nov. and H. huttiense subsp. putei subsp. nov., comb. nov., and description of Herbaspirillum aquaticum sp. nov. Int J Syst Evol Microbiol 60:1418–1426

    Article  PubMed  Google Scholar 

  • Dodsworth JA, Leigh JA (2006) Regulation of nitrogenase by 2-oxoglutarate-reversible, direct binding of a PII-like nitrogen sensor protein to dinitrogenase. Proc Natl Acad Sci USA 103:9779–9784

    Article  PubMed  CAS  Google Scholar 

  • Drepper T, Gross S, Yakunin AF, Hallenbeck PC, 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

    Article  PubMed  CAS  Google Scholar 

  • Elbeltagy A, Nishioka K, Sato T, Suzuki H, Ye B, Hamada T, Isawa T, Mitsui H, Minamisawa K (2001) Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl Environ Microbiol 67:5285–5293

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Fu H, Burris RH (1989) Ammonium inhibition of nitrogenase activity in Herbaspirillum seropedicae. J Bacteriol 171:3168–3175

    PubMed  CAS  Google Scholar 

  • Gunsalus RP, Park SJ (1994) Aerobic-anaerobic gene regulation in Escherichia coli: control by the ArcAB and Fnr regulons. Res Microbiol 145:437–450

    Article  PubMed  CAS  Google Scholar 

  • Gusso CL, Souza EM, Rigo LU, Pedrosa FO, Yates MG, Rego FGM, Klassen G (2008) Effect of an ntrC mutation on amino acid or urea utilization and on nitrogenase switch-off in Herbaspirillum seropedicae. Can J Microbiol 54:235–239

    Article  PubMed  CAS  Google Scholar 

  • Gyaneshwar P, James EK, Reddy PM, Ladha JK (2002) Herbaspirillum colonization increases growth and nitrogen accumulation in aluminium tolerant rice varieties. New Phytol 154:131–146

    Article  CAS  Google Scholar 

  • Hageman RV, Burris RH (1978) Nitrogenase and nitrogenase reductase associate and dissociate with each catalytic cycle. Proc Natl Acad Sci USA 75:2699–26702

    Article  PubMed  CAS  Google Scholar 

  • Hernandez JA, Igarashi RY, Soboh B, Curatti L, Dean DR, Ludden PW, Rubio LM (2007) NifX and NifEN exchange NifB cofactor and the VK-cluster, a newly isolated intermediate of the iron-molybdenum cofactor biosynthetic pathway. Mol Microbiol 63:177–192

    Article  PubMed  CAS  Google Scholar 

  • Huergo LF, Souza EM, Araujo MS, Pedrosa FO, Chubatsu LS, Steffens MBR, Merrick M (2006) ADP-ribosylation of dinitrogenase reductase in Azospirillum brasilense is regulated by AmtB-dependent membrane sequestration of DraG. Mol Microbiol 59:326–337

    Article  PubMed  CAS  Google Scholar 

  • Huergo LF, Merrick M, Monteiro RA, Chubatsu LS, Steffens MB, Pedrosa FO, Souza EM (2009) In vitro interactions between the PII proteins and the nitrogenase regulatory enzymes dinitrogenase reductase ADP-ribosyltransferase (DraT) and dinitrogenase reductase-activating glycohydrolase (DraG) in Azospirillum brasilense. J Biol Chem 284:6674–6682

    Article  PubMed  CAS  Google Scholar 

  • Huergo LF, Noindorf L, Gimenes C, Lemgruber RSP, Cordelini DF, Falarz J, Cruz LM, Monteiro RA, Pedora FO, Chubatsu LS, Souza EM, Steffens MBR (2010) Proteomic analysis of Herbaspirillum seropedicae reveals ammonium-induced AmtB-dependent membrane sequestration of PII proteins. FEMS Microbiol Lett 308:40–47

    Article  PubMed  CAS  Google Scholar 

  • Im WT, Bae HS, Yokota A, Lee ST (2004) Herbaspirillum chlorophenolicum sp. nov., a 4-chlorophenol-degrading bacterium. Int J Syst Evol Microbiol 54:851–855

    Article  PubMed  CAS  Google Scholar 

  • James EK, Olivares FL (1998) Infection and colonization of sugar cane and other graminaceous plants by endophytic diazotrophs. Crit Rev Plant Sci 17:77–119

    Article  Google Scholar 

  • James EK, Gyaneshwar P, Mathan N, Barraquio WL, Reddy PM, Iannetta PP, Olivares FL, Ladha JK (2002) Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Mol Plant Microbe Interact 15:894–906

    Article  PubMed  CAS  Google Scholar 

  • Jung SY, Lee MH, Oh TK, Yoon JH (2007) Herbaspirillum rhizosphaerae sp. nov., isolated from rhizosphere soil of Allium victorialis var. platyphyllum. Int J Syst Evol Microbiol 57:2284–2288

    Article  PubMed  CAS  Google Scholar 

  • Kirchhof G, Eckert B, Stoffels M, Baldani JI, Reis VM, Hartmann A (2001) Herbaspirillum frisingense sp. nov., a new nitrogen-fixing bacterial species that occurs in C4-fibre plants. Int J Syst Evol Microbiol 51:157–168

    PubMed  CAS  Google Scholar 

  • Klassen G, Pedrosa FO, Souza EM, Funayama S, Rigo LU (1997) Effect of nitrogen compounds on nitrogenase activity in Herbaspirillum seropedicae SMR1. Can J Microbiol 43:887–891

    Article  CAS  Google Scholar 

  • Klassen G, Pedrosa FO, Souza EM, Yates MG, Rigo LU (1999) Sequencing and functional analysis of the nifENXorf1orf2 gene cluster of Herbaspirillum seropedicae. FEMS Microbiol Lett 181:165–170

    Article  PubMed  CAS  Google Scholar 

  • Klassen G, Pedrosa FO, Souza EM, Yates MG, Rigo LU (2003) Nitrogenase activity of Herbaspirillum seropedicae grown under low iron levels requires the products of nifXorf1 genes. FEMS Microbiol Lett 224:255–259

    Article  PubMed  CAS  Google Scholar 

  • Little R, Colombo V, Leech A, Dixon R (2002) Direct Interaction of the regulatory NifL protein with the GlnK signal transducer enables the Azotobacter vinelandii NifL-NifA regulatory system to respond to conditions replete for nitrogen. J Biol Chem 277:15472–15481

    Article  PubMed  CAS  Google Scholar 

  • Machado IM, Yates MG, Machado HB, Souza EM, Pedrosa FO (1996) Cloning and sequencing of the nitrogenase structural genes nifHDK of Herbaspirillum seropedicae. Braz J Med Biol Res 29:1599–1602

    PubMed  CAS  Google Scholar 

  • Martin DE, 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

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Argudo I, Little R, Shearer N, Johnson P, Dixon R (2004) The NifL-NifA System: a multidomain transcripion regulatory complex that integrates environmental signals. J Bacteriol 186:601–610

    Article  PubMed  CAS  Google Scholar 

  • Merrick MJ, Edwards RA (1995) Nitrogen control in bacteria. Microbiol Rev 59:604–622

    PubMed  CAS  Google Scholar 

  • Minchin SD, Austin S, Dixon RA (1988) The role of activator binding sites in transcriptional control of the divergently transcribed nifF and nifLA promoters from Klebsiella pneumoniae. Mol Microbiol 2:433–442

    Article  PubMed  CAS  Google Scholar 

  • Monteiro RA, Souza EM, Funayama S, Yates MG, Pedrosa FO, Chubatsu LS (1999a) Expression and functional analysis of an N-truncated NifA protein of Herbaspirillum seropedicae. FEBS Lett 447:283–286

    Article  PubMed  CAS  Google Scholar 

  • Monteiro RA, Souza EM, Yates MG, Pedrosa FO, Chubatsu LS (1999b) In-trans regulation of the N-truncated-NIFA protein of Herbaspirillum seropedicae by the N-terminal domain. FEMS Microbiol Lett 180:157–161

    Article  PubMed  CAS  Google Scholar 

  • Monteiro RA, Souza EM, Yates MG, Steffens MBR, Pedrosa FO, Chubatsu LS (2003a) Expression, purification, and functional analysis of the C-terminal domain of Herbaspirillum seropedicae NifA protein. Protein Expr Purif 27:313–318

    Article  PubMed  CAS  Google Scholar 

  • Monteiro RA, Souza EM, Yates MG, Pedrosa FO, Chubatsu LS (2003b) Fnr is involved in oxygen control of Herbaspirillum seropedicae N-truncated NifA protein activity in Escherichia coli. Appl Environ Microbiol 69:1527–1531

    Article  PubMed  CAS  Google Scholar 

  • Moreno-Vivian C, Schmehl M, Masephol B, Arnold W, Klipp W (1989) DNA sequence and genetic analysis of the Rhodobacter capsulatus nifENX gene region: homology between NifX and NifB suggests involvement of NifX in processing of the iron-molybdenum cofactor. Mol Gen Genet 216:353–363

    Article  PubMed  CAS  Google Scholar 

  • Ninfa AJ, Jiang P, Atkinson MR, Peliska JA (2000) Integration of antagonistic signals in the regulation of nitrogen assimilation in Escherichia coli. Curr Top Cell Regul 36:31–75

    Article  PubMed  CAS  Google Scholar 

  • Noindorf L, Rego FGM, Baura VA, Monteiro RA, Wassem R, Cruz LM, Rigo LU, Souza EM, Steffens MBR, Pedrosa FO, Chubatsu LS (2006) Characterization of the orf1glnKamtB operon of Herbaspirillum seropedicae. Arch Microbiol 185:55–62

    Article  PubMed  CAS  Google Scholar 

  • Noindorf L, Bonatto AC, Monteiro RA, Souza EM, Rigo LU, Pedrosa FO, Steffens MBR, Chubatsu LS (2011) Role of PII proteins in nitrogen fixation control of Herbaspirillum seropedicae strain SmR1. BMC Microbiol 11:1–8

    Article  Google Scholar 

  • Olivares FL, Baldani VLD, Reis V, Baldani JI, Dobereiner J (1996) Occurrence of the endophytic diazotrophs Herbaspirillum spp. in roots, stems, and leaves, predominantly of Gramineae. Biol Fertil Soils 21:197–200

    Article  Google Scholar 

  • Oliveira MAS, Baura VA, Aquino B, Huergo LF, Kadowaki MAS, Chubatsu LS, Souza EM, Dixon R, Pedrosa FO, Wassem R, Monteiro RA (2009) Role of conserved cysteine residues in Herbaspirillum seropedicae NifA activity. Res Microbiol 160:389–395

    Article  PubMed  CAS  Google Scholar 

  • Pedrosa FO, Benelli EM, Yates MG, Wassem R, Monteiro RA, Klassen G, Steffens MBR, Souza EM, Chubatsu LS, Rigo LU (2001) Recent developments in the structural organization and regulation of nitrogen fixation genes in Herbaspirillum seropedicae. J Biotechnol 91:189–195

    Article  PubMed  CAS  Google Scholar 

  • Pedrosa FO, Monteiro RA, Wassem R et al. (2011) Genome of Herbaspirillum seropedicae strain SmR1, a specialized diazotrophic endophyte of tropical grass. PLoS Genetics 7:e1002064

    Google Scholar 

  • Persuhn DC, Souza EM, Steffens MBR, Pedrosa FO, Yates MG, Rigo LU (2000) The transcriptional activator NtrC controls the expression and activity of glutamine synthetase in Herbaspirillum seropedicae. FEMS Microbiol Lett 192:217–221

    Article  PubMed  CAS  Google Scholar 

  • Rees DC, Tezcan FA, Haynes CA, Walton MY, Andrade S, Einsle O, Howard JB (2005) Structural basis of biological nitrogen fixation. Philos Trans R Soc Lond A 363:971–984

    Article  CAS  Google Scholar 

  • Rego FGM, Pedrosa FO, Chubatsu LS, Yates MG, Wassem R, Steffens MBR, Rigo LU, Souza EM (2006) The expression of nifB gene from Herbaspirillum seropedicae is dependent upon the NifA and RpoN proteins. Can J Microbiol 52:1199–1207

    Article  PubMed  CAS  Google Scholar 

  • Roncato-Maccari LD, Ramos HJ, Pedrosa FO, Alquini Y, Chubatsu LS, Yates MG, Rigo LU, Steffens MB, Souza EM (2003) Endophytic Herbaspirillum seropedicae expresses nif genes in gramineous plants. FEMS Microbiol Ecol 45:39–47

    Article  PubMed  CAS  Google Scholar 

  • Rosconi F, Souza EM, Pedrosa FO, Platero RA, González C, González M, Batista S, Gill PR, Fabiano ER (2006) Iron depletion affects nitrogenase activity and expression of nifH and nifA genes in Herbaspirillum seropedicae. FEMS Microbiol Lett 258:214–219

    Article  PubMed  CAS  Google Scholar 

  • Rothballer M, Schmid M, Klein I, Gattinger A, Grundmann S, Hartmann A (2006) Herbaspirillum hiltneri sp. nov., isolated from surface-sterilized wheat roots. Int J Syst Evol Microbiol 56:1341–1348

    Article  PubMed  CAS  Google Scholar 

  • Schwab S, Souza EM, Yates MG, Persuhn DC, Steffens MBR, Chubatsu LS, Pedrosa FO, Rigo LU (2007) The glnAntrBC operon of Herbaspirillum seropedicae is transcribed by two oppositely regulated promoters upstream of glnA. Can J Microbiol 53:100–105

    Article  PubMed  CAS  Google Scholar 

  • Souza EM, Funayama S, Rigo LU, Pedrosa FO (1991a) Cloning and characterization of the nifA gene from Herbaspirillum seropedicae strain Z78. Can J Microbiol 37:425–429

    Article  PubMed  CAS  Google Scholar 

  • Souza EM, Funayama S, Rigo LU, Yates MG, Pedrosa FO (1991b) Sequence and structural organization of a nifA-like gene and part of a nifB-like gene of Herbaspirillum seropedicae strain Z78. J Gen Microbiol 137:1511–1522

    PubMed  CAS  Google Scholar 

  • Souza EM, Pedrosa FO, Drummond M, Rigo LU, Yates MG (1999) Control of Herbaspirillum seropedicae NifA activity by ammonium ions and oxygen. J Bacteriol 181:681–684

    PubMed  CAS  Google Scholar 

  • Souza EM, Pedrosa FO, Rigo LU, Machado HB, Yates MG (2000) Expression of the nifA gene of Herbaspirillum seropedicae: role of the NtrC and NifA binding sites and of the −24/-12 promoter element. Microbiology 146:1407–1418

    PubMed  CAS  Google Scholar 

  • Souza AL, Invitti AL, Rego FG, Monteiro RA, Klassen G, Souza EM, Chubatsu LS, Pedrosa FO, Rigo LU (2010) The involvement of nif associated ferrodoxin-like genes fdxA and fdxN of Herbaspirillum seropedicae in nitrogen fixation. J Microbiol 48:77–83

    Article  PubMed  CAS  Google Scholar 

  • Tremblay PL, Hallenbeck PC (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

    Article  PubMed  CAS  Google Scholar 

  • Valverde A, Velázquez E, Gutiérrez C, Cervantes E, Ventosa A, Igual JM (2003) Herbaspirillum lusitanum sp. nov., a novel nitrogen-fixing bacterium associated with root nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol 53:1979–1983

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Franke CC, Nordlund S, Norén A (2005) Reversible membrane association of dinitrogenase reductase activating glycohydrolase in the regulation of nitrogenase activity in Rhodospirillum rubrum; dependence on GlnJ and AmtB1. FEMS Microbiol Lett 253:273–279

    Article  PubMed  CAS  Google Scholar 

  • Wassem R, Souza EM, Yates MG, Pedrosa FO, Buck M (2000) Two roles for integration host factor at an enhancer-dependent nifA promoter. Mol Microbiol 35:756–764

    Article  PubMed  CAS  Google Scholar 

  • Wassem R, Pedrosa FO, Yates MG, Rego FGM, Chubatsu LS, Rigo LU, Souza EM (2002) Control of autogenous activation of Herbaspirillum seropedicae nifA promoter by the IHF protein. FEMS Microbiol Lett 212:177–182

    Article  PubMed  CAS  Google Scholar 

  • Wigneshweraraj S, Bose D, Burrows PC, Joly N, Schumacher J, Rappas M, Pape T, Zhang X, Stockley P, Severinov K, Buck M (2008) Modus operandi of the bacterial RNA polymerase containing the sigma 54 promoter-specificity factor. Mol Microbiol 68:538–546

    Article  PubMed  CAS  Google Scholar 

  • Xu Y, Cheah E, Carr PD, van Heeswijk WC, Westerhoff HV, Vasudevan SG, Ollis DL (1998) GlnK, a PII-homologue: structure reveals ATP binding site and indicates how the T-loops may be involved in molecular recognition. J Mol Biol 282:149–165

    Article  PubMed  CAS  Google Scholar 

  • Yakunin AF, Hallenbeck PC (2002) AmtB is necessary for NH +4 -induced nitrogenase switch-off and ADP-ribosylation in Rhodobacter capsulatus. J Bacteriol 184:4081–4088

    Article  PubMed  CAS  Google Scholar 

  • Zamaroczy M, Paquelin A, Elmerich C (1993) Functional organization of the glnB-glnA cluster of Azospirillum brasilense. J Bacteriol 175:2507–2515

    PubMed  Google Scholar 

  • Zhang Y, Pohlmann EL, Ludden PW, Roberts GP (2000) Mutagenesis and functional characterization of the glnB, glnA, and nifA genes from the photosynthetic bacterium Rhodospirillum rubrum. J Bacteriol 182:983–992

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Wolfe DM, Pohlmann EL, Conrad MC, Roberts GP (2006) Effect of AmtB homologues on the post-translational regulation of nitrogenase activity in response to ammonium and energy signals in Rhodospirillum rubrum. Microbiology 152:2075–2089

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Dr. Ray Dixon for critical reading of the manuscript. We are also grateful to Roseli Prado, Valter de Baura, Marilza Lamour and Julieta Pie for technical assistance. This work was supported by INCT-FBN/CNPq/MCT, Institutos do Milênio, PRONEX, CAPES, CNPq and Fundação Araucária

Author information

Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, Universidade Federal do Paraná, CP 19046, Curitiba, PR, 81531–980, Brazil

    Leda Satie Chubatsu, Rose Adele Monteiro, Emanuel Maltempi de Souza, Marco Aurelio Schuler de Oliveira, Marshall Geoffrey Yates, Luciano Fernandes Huergo, Maria Berenice Reynaud Steffens, Liu Un Rigo & Fabio de Oliveira Pedrosa

  2. Department of Genetics, Universidade Federal do Paraná, CP 19071, Curitiba, PR, 81531–980, Brazil

    Roseli Wassem & Ana Claudia Bonatto

Authors
  1. Leda Satie Chubatsu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rose Adele Monteiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Emanuel Maltempi de Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marco Aurelio Schuler de Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marshall Geoffrey Yates
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Roseli Wassem
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ana Claudia Bonatto
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Luciano Fernandes Huergo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Maria Berenice Reynaud Steffens
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Liu Un Rigo
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Fabio de Oliveira Pedrosa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Leda Satie Chubatsu.

Additional information

Responsible Editor: Euan K. James.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chubatsu, L.S., Monteiro, R.A., de Souza, E.M. et al. Nitrogen fixation control in Herbaspirillum seropedicae . Plant Soil 356, 197–207 (2012). https://doi.org/10.1007/s11104-011-0819-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-011-0819-6

Keywords

Search

Navigation