Skip to main content
SpringerLink
Log in

The Mechanism of Symbiotic Nitrogen Fixation

  • Chapter
  • First Online:
The Mechanistic Benefits of Microbial Symbionts

Part of the book series: Advances in Environmental Microbiology ((AEM,volume 2))

Abstract

Nitrogen is a building block of life. Molecular nitrogen is the relatively inert atmospheric form of this element, and it must be fixed into more biologically accessible forms in order to be used for organic processes. In total, approximately 380 teragrams of nitrogen per year are fixed by atmospheric, biological, and industrial nitrogen fixation processes. Whereas the Haber–Bosch process currently accounts for the majority of the reduced nitrogen that is used agriculturally with the world’s increasing dependence on agriculture to feed its population, the use of reduced nitrogen derived from energy provided by fossil fuels in not likely to be sustainable. Biological nitrogen fixation is mediated by diazotrophic microorganisms that are capable of fixing atmospheric nitrogen using the enzyme nitrogenase. Much of this is carried out as a symbiotic association between plants and some diazotrophic bacteria. The study of symbiotic nitrogen fixation is an area of research that spans both microbiology and plant biology. Since this is an area that has had a great deal of renewed interest, this chapter reviews what is currently understood about the process of symbiotic nitrogen fixation at the molecular and physiological level from both the plant and bacterial perspective.

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

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
eBook
USD 129.00
Price excludes VAT (USA)
Softcover Book
USD 169.99
Price excludes VAT (USA)
Hardcover Book
USD 169.99
Price excludes VAT (USA)

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Allison FE (1935) Carbohydrate supply as a primary factor in legume symbiosis. Soil Sci 39:123–143

    Article  CAS  Google Scholar 

  • Amor BB et al (2003) The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation. Plant J 34:495–506

    Article  PubMed  Google Scholar 

  • Ané J-M et al (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364–1367

    Article  PubMed  CAS  Google Scholar 

  • Anthamatten D, Hennecke H (1991) The regulatory status of the fixL-like and fixJ-like genes in Bradyrhizobium japonicum may be different from that in Rhizobium meliloti. Mol Gen Genet 225:38–48

    Article  CAS  PubMed  Google Scholar 

  • Anthamatten D, Scherb B, Hennecke H (1992) Characterization of a fixLJ-regulated Bradyrhizobium japonicum gene sharing similarity with the Escherichia coli fnr and Rhizobium meliloti fixK genes. J Bacteriol 174:2111–2120

    CAS  PubMed  PubMed Central  Google Scholar 

  • Appleby CA (1984) Leghemoglobin and Rhizobium respiration. Ann Rev Plant Physiol 35:443–478

    Article  CAS  Google Scholar 

  • Ardissone S et al (2011) Role of BacA in lipopolysaccharide synthesis, peptide transport, and nodulation by Rhizobium sp. strain NGR234. J Bacteriol 193:2218–2228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ardourel M et al (1995) In Rhizobium meliloti, the operon associated with the nod box n5 comprises nodL, noeA and noeB, three host-range genes specifically required for the nodulation of particular Medicago species. Mol Microbiol 17:687–699

    Article  CAS  PubMed  Google Scholar 

  • Atkinson EM, Palcic MM, Hindsgaul O, Long SR (1994) Biosynthesis of Rhizobium meliloti lipooligosaccharide Nod factors: NodA is required for an N-acyltransferase activity. Proc Natl Acad Sci U S A 91:8418–8422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barnett MJ et al (2001) Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid. Proc Natl Acad Sci U S A 98:9883–9888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barsch A, Carvalho HG, Cullimore JV, Niehaus K (2006) GC–MS based metabolite profiling implies three interdependent ways of ammonium assimilation in Medicago truncatula root nodules. J Biotechnol 127:79–83

    Article  CAS  PubMed  Google Scholar 

  • Bauer E, Kaspar T, Fisher 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Benson DR, Silvester W (1993) Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Rev 57:293–311

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bergersen FJ, Goodchild DJ (1973) Aeration pathways in soybean root nodules. Aust J Biol Sci 26:729–740

    Article  Google Scholar 

  • Bergersen FJ, Turner GL (1993) Effects of concentrations of substrates supplied to N2 fixing soybean bacteroids in flow chamber reaction. Proc R Soc Lond Ser B 251:103–109

    Article  Google Scholar 

  • Burgess BK (1984) Structure and reactivity of nitrogenase-an overview. In: Ludden PW, Burris JE (eds) Advances in nitrogen fixation research. Elsevier, New York, NY, pp 66–74

    Google Scholar 

  • Campbell GR, Reuhs BL, Walker GC (2002) Chronic intracellular infection of alfalfa nodules by Sinorhizobium meliloti requires correct lipopolysaccharide core. Proc Natl Acad Sci U S A 99:3938–3943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Capela D et al (2001) Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti strain 1021. Proc Natl Acad Sci U S A 98:9877–9882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Catoira R et al (2000) Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12:1647–1665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan MK, Kim J, Rees DC (1993) The nitrogenase FeMo-cofactor and P-cluster pair: 2.2 angstrom resolution. Science 260:792–794

    Article  CAS  PubMed  Google Scholar 

  • Cheng HP, Walker GC (1998) Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J Bacteriol 180:5183–5191

    CAS  PubMed  PubMed Central  Google Scholar 

  • Copeland L, Quinell RG, Day DA (1989) Malic enzyme in bacteroids from soybean nodules. J Gen Microbiol 135:2005–2011

    CAS  Google Scholar 

  • Cordoba E, Shishkova S, Vance CP, Hernández G (2003) Antisense inhibition of NADH glutamate synthase impairs carbon/nitrogen assimilation in nodules of alfalfa (Medicago sativa L.). Plant J 33:1037–1049

    Article  CAS  PubMed  Google Scholar 

  • Dakora FA, Atkins CA (1990) Morphological and structural adaptation of nodules of cowpea to functioning under sub- and supra-ambient O2 pressure. Planta 182:572–582

    Article  CAS  PubMed  Google Scholar 

  • David M et al (1988) Cascade regulation of nif gene expression in Rhizobium meliloti. Cell 54:671–683

    Article  CAS  PubMed  Google Scholar 

  • Day DA, Poole PS, Tyerman SD, Rosendahl L (2001) Ammonia and amino acid transport across symbiotic membranes in nitrogen-fixing legume nodules. Cell Mol Life Sci 58(1):61–71

    Article  CAS  PubMed  Google Scholar 

  • de Philip P, Batut J, Boistard P (1990) Rhizobium meliloti FixL is an oxygen sensor and regulates R. meliloti nifA and fixK genes differently in Escherichia coli. J Bacteriol 172:4255–4262

    PubMed  PubMed Central  Google Scholar 

  • Demont N, Debellé F, Aurelle H, Dénarié J, Promé J (1993) Role of the Rhizobium meliloti nodF and nodE genes in the biosynthesis of lipo-oligosaccharidic nodulation factors. J Biol Chem 268:20134–20142

    CAS  PubMed  Google Scholar 

  • diCenzo G, Milunovic B, Cheng J, Finan TM (2013) tRNAarg and engA are essential genes on the 1.7 Mb pSymB megaplasmid of Sinorhizobium meliloti and were translocated together from the chromosome in an ancestral strain. J Bacteriol 195:202–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dickstein R, Bisseling T, Reinhold VN, Ausubel FM (1988) Expression of nodule-specific genes in alfalfa root nodules blocked at an early stage of development. Genes Dev 2:677–687

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Downie JA (1994) Signalling strategies for nodulation of legumes by rhizobia. Trends Microbiol 2:318–324

    Article  CAS  PubMed  Google Scholar 

  • Driscoll BT, Finan TM (1993) NAD+-dependent malic enzyme of Rhizobium meliloti is required for symbiotic nitrogen fixation. Mol Microbiol 7:865–873

    Article  CAS  PubMed  Google Scholar 

  • Driscoll BT, Finan TM (1996) NADP+-dependent malic enzyme of Rhizobium meliloti. J Bacteriol 178:2224–2231

    CAS  PubMed  PubMed Central  Google Scholar 

  • Driscoll BT, Finan TM (1997) Properties of NAD+- and NADP+-dependent malic enzymes of Rhizobium (Sinorhizobium) meliloti and differential expression of their genes in nitrogen-fixing bacteroids. Microbiology 143:489–498

    Article  PubMed  Google Scholar 

  • Dunn MF, Araíza G, Finan TM (2001) Cloning and characterization of the pyruvate carboxylase from Sinorhizobium meliloti Rm1021. Arch Microbiol 176:355–363

    Article  CAS  PubMed  Google Scholar 

  • Dylan T et al (1986) Rhizobium meliloti genes required for nodule development are related to chromosomal virulence genes in Agrobacterium tumefaciens. Proc Natl Acad Sci U S A 83:4403–4407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dylan T, Helinski DR, Ditta GS (1990a) Hypoosmotic adaptation in Rhizobium meliloti requires ß-(1-2) glucan synthesis. J Bacteriol 172:1400–1408

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dylan T, Nagpal P, Helinski D, Ditta GS (1990b) Symbiotic pseudorevertants of Rhizobium meliloti ndv mutants. J Bacteriol 172:1409–1417

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dymov SI, Meek DJ, Steven B, Driscoll BT (2004) Insertion of transposon Tn5tac1 in the Sinorhizobium meliloti malate dehydrogenase (mdh) gene results in conditional polar effects on downstream TCA cycle genes. Mol Plant Microbe Interact 17:1318–1327

    Article  CAS  PubMed  Google Scholar 

  • Egelhoff TT, Fisher RF, Jacobs TW, Mulligan JT, Long SR (1985) Nucleotide sequence of Rhizobium meliloti 1021 nodulation genes: nodD is read divergently from nodABC. DNA 4:241–248

    Article  CAS  PubMed  Google Scholar 

  • Ehrhardt DW, Wais R, Long SR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85:673–681

    Article  CAS  PubMed  Google Scholar 

  • Einsle O (2014) Nitrogenase Fe Mo cofactor: atomic structure in three simple steps. J Biol Inorg Chem 19(6):737–745

    Article  CAS  PubMed  Google Scholar 

  • Endre G, Kereszt A, Kevei Z, Mihacea S, Kaló P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962–966

    Article  CAS  PubMed  Google Scholar 

  • Ertl G (1991) Elementary steps in ammonia synthesis. In: Jennings JR (ed) Catalytic ammonia synthesis. Springer US, New York, NY, pp 109–132

    Chapter  Google Scholar 

  • Farkas A et al (2014) Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms. Proc Natl Acad Sci U S A 111:5183–5188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferguson GP, Datta A, Baumgartner J, Roop RM, Carlson RW, Walker GC (2004) Similarity to peroxisomal-membrane protein family reveals that Sinorhizobium and Brucella BacA affect lipid-A fatty acids. Proc Natl Acad Sci U S A 101:5012–5017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finan TM, Wood JM, Jordan DC (1983) Symbiotic properties of C4-dicarboxylic acid transport mutants of Rhizobium leguminosarum. J Bacteriol 154:1403–1413

    CAS  PubMed  PubMed Central  Google Scholar 

  • Finan TM, Kunkel B, de Vos GF, Signer ER (1986) Second symbiotic megaplasmid in Rhizobium meliloti carrying exopolysaccharide and thiamine synthesis genes. J Bacteriol 167:66–72

    CAS  PubMed  PubMed Central  Google Scholar 

  • Finan TM, Oresnik I, Bottacin A (1988) Mutants of Rhizobium meliloti defective in succinate metabolism. J Bacteriol 170:3396–3403

    CAS  PubMed  PubMed Central  Google Scholar 

  • Finan TM, McWhinne E, Driscoll B, Watson RJ (1991) Complex symbiotic phenotypes result from gluconeogenic mutations in Rhizobium meliloti. Mol Plant Microbe Interact 4:386–392

    Article  CAS  Google Scholar 

  • Finan TM et al (2001) The complete sequence of the 1,683-kb pSymB megaplasmid from the N2-fixing endosymbiont S. meliloti. Proc Natl Acad Sci USA 98:9889–9894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Fisher 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  Google Scholar 

  • Fisher RF, Long SR (1993) Interactions of NodD at the nod box: NodD binds to two distinct sites on the same face of the helix and induces a bend in the DNA. J Mol Biol 233:336–348

    Article  CAS  PubMed  Google Scholar 

  • Foussard M, Garnerone AM, Ni F, Soupène E, Boistard P, Batut J (1997) Negative autoregulation of the Rhizobium meliloti fixK gene is indirect and requires a newly identified regulator, FixT. Mol Microbiol 25:27–37

    Article  CAS  PubMed  Google Scholar 

  • Gage DJ (2002) Analysis of infection thread development using Gfp- and DsRed- expressing Sinorhizobium meliloti. J Bacteriol 184:7042–7046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gage DG (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68:280–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gage DJ, Bobo T, Long SR (1996) Use of green fluorescent protein to visualize the early events of symbiosis between Rhizobium meliloti and Alfalfa (Medicago sativa). J Bacteriol 178:7159–7166

    CAS  PubMed  PubMed Central  Google Scholar 

  • Galibert F et al (2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668–672

    Article  CAS  PubMed  Google Scholar 

  • Galloway JN et al (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 760:153–226

    Article  Google Scholar 

  • Galloway JN et al (2008) Transformation of the nitrogen cycle: recent trends, question, and potential solutions. Science 320:889–892

    Article  CAS  PubMed  Google Scholar 

  • Gardiol A, Arias A, Cerveñansky C, Martinez de Drets G (1982) Succinate dehydrogenase mutant of Rhizobium meliloti. J Bacteriol 151:1621–1623

    CAS  PubMed  PubMed Central  Google Scholar 

  • Geddes BA, Oresnik IJ (2012) Genetic characterization of a complex locus necessary for the transport and catabolism of erythritol, adonitol, and L-arabitol in Sinorhizobium meliloti. Microbiology 158:2180–2191

    Article  CAS  PubMed  Google Scholar 

  • Geddes BA, Gonzalez JE, Oresnik IJ (2014) Exopolysaccharide production in response to medium acidification is correlated with an increase in competition for nodule occupancy. Mol Plant Microbe Interact 27(12):1307–1317

    Article  PubMed  CAS  Google Scholar 

  • Georgiadis MM, Komiya H, Chakrabarti P, Woo D, Kornuc JJ, Rees DC (1992) Crystallographic structure of the nitrogenase iron protein from Azotobacter vinelandii. Science 257:1653–1659

    Article  CAS  PubMed  Google Scholar 

  • Geremia RA, Cavaignac S, Zorreguieta A, Toro N, Olivares J, Ugalde R (1987) A Rhizobium meliloti mutant that forms ineffective pseudonodules in alfalfa produces exopolysaccharide but fails to form β-(1-2) glucan. J Bacteriol 169:880–884

    CAS  PubMed  PubMed Central  Google Scholar 

  • Geremia RA, Mergaert P, Geelen D, Van Montagu M, Holsters M (1994) The NodC protein of Azorhizobium caulinodans is an N-acetylglucosaminyltransferase. Proc Natl Acad Sci U S A 91:2669–2673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilles-Gonzalez MA, Ditta GS, Helinski DR (1991) A haemoprotein with kinase activity encoded by the oxygen sensor of Rhizobium meliloti. Nature 350:170–172

    Article  CAS  PubMed  Google Scholar 

  • Giraud E et al (2007) Legume symbiosis: absence of nod genes in photosynthetic Bradyrhizobia. Science 316:1307–1312

    Article  PubMed  Google Scholar 

  • Glazebrook J, Walker GC (1989) A novel exopolysaccharide can function in place of calcofluor-binding exopolysaccharide in nodulation on alfalfa. Cell 56:661–672

    Article  CAS  PubMed  Google Scholar 

  • Glazebrook J, Ichige A, Walker GC (1993) A Rhizobium meliloti homolog of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroid development. Genes Dev 7:1485–1497

    Article  CAS  PubMed  Google Scholar 

  • Gleason C, Chaudhuri S, Yang T, Muñoz A, Poovaiah B, Oldroyd GE (2006) Nodulation independent of rhizobia induced by a calcium-activated kinase lacking auto-inhibition. Nature 441:1149–1152

    Article  CAS  PubMed  Google Scholar 

  • Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311:1–18

    Article  CAS  Google Scholar 

  • Hirsch S, Kim J, Muñoz A, Heckmann AB, Downie JA, Oldroyd GE (2009) GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21:545–557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Honma M, Asomaning M, Ausubel FM (1990) Rhizobium meliloti nodD genes mediate host-specific activation of nodABC. J Bacteriol 172:901–911

    CAS  PubMed  PubMed Central  Google Scholar 

  • Horváth B et al (2011) Medicago truncatula IPD3 is a member of the common symbiotic signaling pathway required for rhizobial and mycorrhizal symbioses. Mol Plant Microbe Interact 24:1345–1358

    Article  PubMed  Google Scholar 

  • Hu Y, Ribbe MW (2013) Nitrogenase assembly. Biochim Biophys Acta 1827:1112–1122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hunt S, Layzell DB (1993) Gas exchange of legume nodules and the regulation of nitrogenase activity. Annu Rev Plant Physiol Plant Mol Biol 44:483–511

    Article  CAS  Google Scholar 

  • Hunt S, Gaito ST, Layzell DB (1987a) Model of gas exchange and diffusion in legume nodules. II. Characterization of the diffusion barrier and estimation of the concentrations of CO2, H2, and N2 in infected cells. Planta 173:128–141

    Article  Google Scholar 

  • Hunt S, King BJ, Canvin DT, Layzell DB (1987b) Steady and non-steady state gas exchange characteristics of soybean nodules in relation to the oxygen diffusion barrier. Plant Physiol 84:164–172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang J, Gu BH, Albright LM, Nixon TB (1989) Conservation between coding and regulatory elements of Rhizobium meliloti and Rhizobium leguminosarum dct genes. J Bacteriol 171:5244–5253

    CAS  PubMed  PubMed Central  Google Scholar 

  • John M, Röhrig H, Schmidt J, Wieneke U, Schell J (1993) Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase. Proc Natl Acad Sci USA 90:625–629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 5:619–633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones KM, Sharopova N, Lohar DP, Zhang JQ, VandenBosch KA, Walker GC (2008) Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant. Proc Natl Acad Sci U S A 105:704–709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jumas-Bilak E, Michaux-Charachon S, Bourg S, Ramuz M, Allardet-Servent A (1998) Unconventional genomic organization in the α subgroup of the Proteobacteria. J Bacteriol 180:2749–2755

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kondorosi E, Buire M, Cren M, Iyer N, Hoffmann B, Kondorosi A (1991) Involvement of the syrM and nodD3 genes of Rhizobium meliloti in nod gene activation and in optimal nodulation of the plant host. Mol Microbiol 5:3035–3048

    Article  CAS  PubMed  Google Scholar 

  • Kouchi H, Yoneyama T (1984a) Dynamics of carbon photosynthetically assimilated in nodulated soybean plants under steady state conditions. 1. Development and applications of 13CO2 assimilation system at a constant 13C abundance. Ann Bot 53:875–882

    CAS  Google Scholar 

  • Kouchi H, Yoneyama T (1984b) Dynamics of carbon photosynthetically assimilated in nodulated soybean plants under steady state conditions. 2. The incorporation of 13C into carbohydrates, organic acids, amino acids, and some storage compounds. Ann Bot 53:883–896

    CAS  Google Scholar 

  • Kouchi H, Yoneyama T (1985) Dynamics of carbon photosynthetically assimilated in nodulated soybean plants under steady state conditions. 3. Time course on 13C incorporation into soluble metabolites and respiratory evolution of 13CO2 from roots and nodules. Ann Bot 56:333–346

    CAS  Google Scholar 

  • Kouchi H, Yoneyama T (1986) Metabolism of 13C-labelled photosynthate in plant cytosol and bacteroids of root nodules of Glycine max. Physiol Plant 68:2338–2344

    Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kuzma MM, Winter H, Storer P, Oresnik IJ, Atkins CA, Layzell DB (1999) The site of oxygen limitation in soybean nodules. Plant Physiol 119:399–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lehman AP, Long SR (2013) Exopolysaccharides from Sinorhizobium meliloti can protect against H2O2-dependent damage. J Bacteriol 195:5362–5369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lerouge P et al (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344:781–784

    Article  CAS  PubMed  Google Scholar 

  • Lévy J et al (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364

    Article  PubMed  CAS  Google Scholar 

  • Liang Y et al (2013) Nonlegumes respond to rhizobial Nod factors by suppressing the innate immune response. Science 341:1384–1387

    Article  CAS  PubMed  Google Scholar 

  • Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R (2003) LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302:630–633

    Article  CAS  PubMed  Google Scholar 

  • Limpens E et al (2005) Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2. Proc Natl Acad Sci U S A 102:10375–10380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lodwig E, Poole P (2003) Metabolism of Rhizobium bacteroids. Crit Rev Plant Sci 22:37–78

    Article  CAS  Google Scholar 

  • Lodwig EM et al (2003) Amino-acid cycling drives nitrogen fixation in the legume-Rhizobium symbiosis. Nature 422:722–726

    Article  CAS  PubMed  Google Scholar 

  • Lois AF, Weinstein M, Ditta GS, Helinski D (1993) Autophosphorylation and phosphatase activities of the oxygen-sensing protein FixL of Rhizobium meliloti are coordinately regulated by oxygen. J Biol Chem 268:4370–4375

    CAS  PubMed  Google Scholar 

  • Madsen EB et al (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637–640

    Article  CAS  PubMed  Google Scholar 

  • Marlow VL et al (2009) Essential role for the BacA protein in the uptake of a truncated eukaryotic peptide in Sinorhizobium meliloti. J Bacteriol 191:1519–1527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marsh JF et al (2007) Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol 144:324–335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masson-Boivin C, Giraud E, Perret X, Batut J (2009) Establishing nitrogen-fixing symbiosis with legumes: how many recipes? Trends Microbiol 17:458–466

    Article  CAS  PubMed  Google Scholar 

  • McDermott TR, Kahn ML (1992) Cloning and mutagenesis of the Rhizobium meliloti isocitrate dehydrogenase gene. J Bacteriol 174(14):4790–4797

    CAS  PubMed  PubMed Central  Google Scholar 

  • McKay IA, Dilworth MJ, Glenn AR (1988) C4-dicarboxylate metabolism in free-living and bacteroid forms of Rhizobium leguminosarum MNF3841. J Gen Microbiol 134:1433–1440

    CAS  Google Scholar 

  • Mergaert P et al (2003) A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs. Plant Physiol 132:161–173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mergaert P et al (2006) Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium–legume symbiosis. Proc Natl Acad Sci U S A 103:5230–5235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mesa S, Hauser F, Friberg M, Malaguti E, Fischer HM, Hennecke H (2008) Comprehensive assessment of the regulons controlled by the FixLJ-FixK2-FixK1 cascade in Bradyrhizobium japonicum. J Bacteriol 190:6568–6579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Middleton PH et al (2007) An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell 19:1221–1234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller JM, Wood JM (1996) Osmoadaptation by rhizosphere bacteria. Annu Rev Microbiol 50:101–136

    Article  CAS  PubMed  Google Scholar 

  • Miller SS, Driscoll BT, Gregerson RG, Gantt JS, Vance CP (1998) Alfalfa malate dehydrogenase (MDH): molecular cloning and characterization of five different forms reveals a unique nodule-enhanced MDH. Plant J 15:173–184

    Article  CAS  PubMed  Google Scholar 

  • Mitsch MJ, Cowie A, Finan TM (2007) Malic enzyme cofactor and domain requirements for symbiotic N2 fixation by Sinorhizobium meliloti. J Bacteriol 189:160–168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morieri G et al (2013) Host-specific Nod-factors associated with Medicago truncatula nodule infection differentially induce calcium influx and calcium spiking in root hairs. New Phytol 200:656–662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muñoz JA, Coronado C, Pérez-Hormaeche J, Kondorosi A, Ratet P, Palomares AJ (1998) MsPG3, a Medicago sativa polygalacturonase gene expressed during the alfalfa-Rhizobium meliloti interaction. Proc Natl Acad Sci U S A 95:9687–9692

    Article  PubMed  PubMed Central  Google Scholar 

  • Noxon J (1976) Atmospheric nitrogen fixation by lightning. Geophys Res Lett 3:463–465

    Article  CAS  Google Scholar 

  • Oldroyd GED, Marray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume-Rhizobial symbiosis. Annu Rev Genet 45:119–144

    Article  CAS  PubMed  Google Scholar 

  • Oresnik IJ, Layzell DB (1994) Composition and distribution of adenylates in soybean (Glycine max L.) nodule tissue. Plant Physiol 104:217–225

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oresnik IJ, Liu SL, Yost CK, Hynes MF (2000) Megaplasmid pRme2011a of Sinorhizobium meliloti is not required for viability. J Bacteriol 182:3582–3586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ott T et al (2009) Absence of symbiotic leghemoglobins alters bacteroid and plant cell differentiation during development of Lotus japonicus root nodules. Mol Plant Microbe Interact 22:800–808

    Article  CAS  PubMed  Google Scholar 

  • Parsons R, Day DA (1990) Mechanism of soybean nodule adaptation to different oxygen pressures. Plant Cell Environ 1990:501–512

    Article  Google Scholar 

  • Perret X, Staehlin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64:180–201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peters NK, Frost JW, Long SR (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:977–980

    Article  CAS  PubMed  Google Scholar 

  • Pierre O, Engler G, Hopkins J, Brau F, Boncompagni E, Hérouart D (2013) Peribacteroid space acidification: a marker of mature bacteroid functioning in Medicago truncatula nodules. Plant Cell Environ 36:2059–2070

    CAS  PubMed  Google Scholar 

  • Poole P, Allaway D (2000) Carbon and nitrogen metabolism in Rhizobium. Adv Microb Physiol 43:117–163

    Article  CAS  PubMed  Google Scholar 

  • Preisig O, Anthamatten D, Hennecke H (1993) Genes for a novel, microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen fixing endosymbiosis. Proc Natl Acad Sci U S A 90:3309–3313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prell J, White JP, Bourdes A, Brunwell S, Bongaerts RJ, Poole PS (2009) Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids. Proc Natl Acad Sci U S A 106:12477–12482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prell J et al (2010) Role of symbiotic auxotrophy in the Rhizobium-legume symbioses. PLoS One 5, e13933

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Radutoiu S et al (2007) LysM domains mediate lipochitin–oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J 26:3923–3935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rastogi VK, Watson RJ (1991) Aspartate aminotransferase activity is required for aspartate catabolism and symbiotic nitrogen fixation in Rhizobium meliloti. J Bacteriol 173:2879–2887

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rawsthorne S, LaRue TA (1986) Preparation and properties of mitochondria from cowpea nodules. Plant Physiol 81:1092–1096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reibach PH, Streeter JG (1983) Metabolism of 14C labelled photosynthate and distribution of enzymes of glucose metabolism in soybean nodules. Plant Physiol 72:634–640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Renalier M et al (1987) A new symbiotic cluster on the pSym megaplasmid of Rhizobium meliloti 2011 carries a functional fix gene repeat and a nod locus. J Bacteriol 169:2231–2238

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reuber TL, Walker GC (1993) Biosynthesis of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti. Cell 74:269–280

    Article  CAS  PubMed  Google Scholar 

  • Robledo M et al (2008) Rhizobium cellulase CelC2 is essential for primary symbiotic infection of legume host roots. Proc Natl Acad Sci U S A 105:7064–7069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roche P et al (1991) Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell 67:1131–1143

    Article  CAS  PubMed  Google Scholar 

  • Röckstrom J et al (2009) A safe operating space for humanity. Nature 461:472–475

    Article  PubMed  CAS  Google Scholar 

  • Ronson CW, Nixon TB, Albright LM, Ausubel FM (1987) Rhizobium meliloti ntrA (rpoN) gene is required for diverse metabolic functions. J Bacteriol 169:2424–2431

    CAS  PubMed  PubMed Central  Google Scholar 

  • Santana MA, Pihakaski-Maunsbach K, Sandal N, Marcker KA, Smith A (1998) Evidence that the plant host synthesizes the heme moiety of leghemoglobin in root nodules. Plant Physiol 116:1259–1269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santos R, Hérouart D, Sigaud S, Touati D, Puppo A (2001) Oxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction. Mol Plant Microbe Interact 14:86–89

    Article  CAS  PubMed  Google Scholar 

  • Schlüter A et al (1997) Functional and regulatory analysis of the two copies of the fixNOQP operon of Rhizobium leguminosarum strain VF39. Mol Plant Microbe Interact 10:605–616

    Article  PubMed  Google Scholar 

  • Sheehy JR, Bergersen FJ, Minchin FR, Witty JF (1987) A simulation study of gaseous diffusion resistance, nodule pressure gradients and biological nitrogen fixation in soybean nodules. Ann Bot 60:345–351

    CAS  Google Scholar 

  • Sinclair TR, Goudriaan J (1981) Physiological constraints of transport in nodules. Plant Physiol 67:143–145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smil V (2000) Enriching the earth: Fritz Haber, Carl Bosch, and the transformation of world food production. MIT Press, Cambridge, MA

    Google Scholar 

  • Spaink HP (2000) Root nodulation and infection factors produced by rhizobial bacteria. Ann Rev Microbiol 54:257–288

    Article  CAS  Google Scholar 

  • Spaink HP, Wijfjes AH, Drift KM, Haverkamp J, Thomas‐Oates JE, Lugtenberg BJ (1994) Structural identification of metabolites produced by the NodB and NodC proteins of Rhizobium leguminosarum. Mol Microbiol 13:821–831

    Article  CAS  PubMed  Google Scholar 

  • Sprent JI (1980) Root nodule anatomy, type of export product and evolutionary origin of some Leguminosae. Plant Cell Environ 3:35–43

    CAS  Google Scholar 

  • Swanson JA, Mulligan JT, Long SR (1993) Regulation of syrM and nodD3 in Rhizobium meliloti. Genetics 134:435–444

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thornley RNF, Lowe DJ (1985) Kinetics and mechanisms of the nitrogenase enzyme system. In: Spiro TJ (ed) Molybdenum enzymes. Wiley, New York, NY, pp 220–284

    Google Scholar 

  • Thumfort PP, Atkins CA, Layzell DB (1994) Re-evaluation of the role of the infected cell in the control of oxygen diffusion in legume nodules. Plant Physiol 105:1321–1333

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thumfort PP, Atkins CA, Layzell DB (2000) A simplified approach for modeling diffusion into cells. J Theor Biol 204:47–65

    Article  CAS  PubMed  Google Scholar 

  • Tjepkema JD, Yocum CS (1974) Measurement of O2 partial pressure within soybean nodules by oxygen electrodes. Planta 119:59–72

    Article  Google Scholar 

  • Udvardi M, Poole PS (2013) Transport and metabolism in legume-Rhizobia symbiosis. Annu Rev Plant Biol 64:781–805

    Article  CAS  PubMed  Google Scholar 

  • Udvardi MK, Price GD, Gresshoff PM, Day DA (1988) A dicarboxylate transporter on the peribacteroid membrane of soybean root nodules. FEBS Lett 231:36–40

    Article  CAS  Google Scholar 

  • Udvardi MK, Yang O, Young S, Day DA (1990) Sugar and amino acid transport across symbiotic membranes of soybean nodules. Mol Plant Microbe Interact 3:334–340

    Article  CAS  Google Scholar 

  • Van de Velde W et al (2010) Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327:1122–1126

    Article  PubMed  CAS  Google Scholar 

  • Vance CP, Heichel GH (1991) Carbon in N2 fixation: limitation or exquisite adaption. Annu Rev Plant Physiol Plant Mol Biol 42:373–392

    Article  CAS  Google Scholar 

  • Vitousek PM (2002) Nitrogen and nature. AMBIO 31:97–101

    Article  PubMed  Google Scholar 

  • Wang D et al (2010) A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science 327:1126–1129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watson RJ, Rastogi VK (1993) Cloning and nucleotide sequencing of Rhizobium meliloti aminotransferase genes: an aspartate aminotransferase required for symbiotic nitrogen fixation is atypical. J Bacteriol 175:1919–1928

    CAS  PubMed  PubMed Central  Google Scholar 

  • Watson RJ, Chan YK, Wheatcroft R, Yang A-F, Han SH (1988) Rhizobium meliloti genes required for C4-dicarboxylate transport and symbiotic nitrogen fixation are located on a megaplasmid. J Bacteriol 170:927–934

    CAS  PubMed  PubMed Central  Google Scholar 

  • Witty JF, Scot L, Revsbech NP (1987) Direct evidence for changes in the resistance of legume root nodules to O2. J Exp Bot 38:1129–1140

    Article  Google Scholar 

  • Yarosh OK, Charles TC, Finan TM (1989) Analysis of C4-dicarboxylate transport genes in Rhizobium meliloti. Mol Microbiol 3:813–823

    Article  CAS  PubMed  Google Scholar 

  • York GM, Walker GC (1998) The succinyl and acetyl modifications of succinoglycan influence susceptibility of succinoglycan to cleavage by the Rhizobium meliloti glycanases ExoK and ExsH. J Bacteriol 180:4184–4191

    CAS  PubMed  PubMed Central  Google Scholar 

  • Young ND et al (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480:520–524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yurgel SN, Kahn ML (2004) Dicarboxylate transport in rhizobia. FEMS Microbiol Rev 28:489–501

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, University of Manitoba, Winnipeg, MB, Canada, R3T 2N2

    Barney A. Geddes & Ivan J. Oresnik

Authors
  1. Barney A. Geddes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ivan J. Oresnik
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ivan J. Oresnik .

Editor information

Editors and Affiliations

  1. Cincinnati, Ohio, USA

    Christon J. Hurst

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Geddes, B.A., Oresnik, I.J. (2016). The Mechanism of Symbiotic Nitrogen Fixation. In: Hurst, C. (eds) The Mechanistic Benefits of Microbial Symbionts. Advances in Environmental Microbiology, vol 2. Springer, Cham. https://doi.org/10.1007/978-3-319-28068-4_4

Download citation

Publish with us

Policies and ethics

Search

Navigation