Skip to main content
SpringerLink
Log in

Ecophysiological aspects of growth and nitrogen fixation inAzospirillum spp.

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

The nitrogenase activity ofAzospirillum spp. is efficiently regulated by environmental factors. InA. brasilense andA. lipoferum a rapid ‘switch off’ of nitrogenase activity occurs after the addition of ammonium chloride. As in photosynthetic bacteria, a covalent modification of nitrogenase reductase (Fe-protein) is involved. InA. amazonense, a non-covalent mechanism causes only a partial inhibition of nitrogenase activity after ammonium chloride is added. In anaerobic conditions, nitrogenase reductase is also ‘switched off’ by a covalent modification inA. brasilense andA. lipoferum. Short-time exposure ofAzospirillum to increased oxygen levels causes a partially reversible inhibition of nitrogenase activity, but no covalent modification is involved.Azospirillum spp. show variations in their oxygen tolerance. High levels of carotenoids confer a slightly improved oxygen tolerance. Certain amino acids (e. g. glutamate, aspartate, histidine and serine) affect growth and nitrogen fixation differently inAzospirillum spp. Amino acids may influence growth and nitrogen fixation ofAzospirillum in the association with plants.Azospirillum brasilense andA. halopraeferens are the more osmotolerant species. They utilize most amino acids poorly and accumulate glycine betaine, which also occurs in osmotically stressed grasses as a compatible solute to counteract osmotic stress. Nitrogen fixation is stimulated by glycine betaine and choline. Efficient iron acquisition is a prerequisite for competitive and aerotoleran growth and for high nitrogenase activity.Azospirillum halopraeferens andA. amazonense assimilate iron reasonably well, whereas growth of someA. brasilense andA. lipoferum strains is severely inhibited by iron limitation and by competition with foreign microbial iron chelators. However, growth of certain iron-limitedA. brasilense strains is stimulated by the phytosiderophore mugineic acid. Thus, various plant-derived substances may stimulate growth and nitrogen fixation ofAzospirillum.

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

Similar content being viewed by others

References

  • Albrecht S L and Okon Y 1980 Cultures ofAzospirillum. Methods Enzymol. 69, 740–749.

    Google Scholar 

  • Bachhawat A K and Gosh S 1987 Iron transport inAzospirillum brasilense: Role of the siderophore spirilobactin. J. Gen. Microbiol. 133, 1759–1765.

    Google Scholar 

  • Balandreau J 1986 Ecological factors and adaptive processes in N2-fixing bacterial populations of the plant environment. Plant and Soil 90, 73–92.

    Google Scholar 

  • Baldani V L D, Alvarez MA de B, Baldani JI and Döbereiner J 1986 Establishment of inoculatedAzospirillum spp. in the rhizosphere and in roots of field grown wheat and sorghum. Plant and Soil 90, 35–46.

    Google Scholar 

  • Bani D C, Barberio M, Favili F, Gallori E and Polsinelli M 1980 Isolation and characterization of glutamate synthase mutants ofAzospirillum brasilense. J. Gen. Microbiol. 119, 239–324.

    Google Scholar 

  • Bossier P and Verstraete W 1986 Detection of siderophores in soil by a direct bioassay. Soil Biol. Biochem. 18, 481–486.

    Google Scholar 

  • Bowdre J H, Krieg N R, Hoffman P S and Smibert R M 1976 Stimulatory effect of dihydroxyphenyl compounds on the aerotolerance ofSpirillum volutans andCampylobacter fetus subspecies jejuni. Appl. Environ. Microbiol. 31, 127–133.

    PubMed  Google Scholar 

  • Braun V 1985 The unusual features of the iron transport systems ofEscherichia coli. Trends Biochem. Sci. 10, 75–78.

    Google Scholar 

  • Brock T D 1985 Procaryotic population ecology.In Engineered Organisms in the Environment: Scientific Issues. Eds. HO Halvorson, D Pramer and M Rogul. pp 176–179. American Society for Microbiology, Washington, D.C.

    Google Scholar 

  • Brown A D 1976 Microbial water stress. Bact. Reviews 40, 803–846.

    Google Scholar 

  • Burris R H 1972 Nitrogen fixation — Assay methods and techniques. Methods Enzymol. 24B, 415–431.

    Google Scholar 

  • Burton G W and Ingold K U 1984 β-Carotene: An unusual type of lipid antioxidant. Science 224, 569–573.

    PubMed  Google Scholar 

  • Clara R W and Knowles R 1985 Superoxide dismutase, catalase and peroxidase in ammonium-grown and nitrogen-fixingAzospirillum brasilense. Can. J. Microbiol. 30, 1222–1228.

    Google Scholar 

  • Curl E A and Truelove B 1986 The Rhizosphere, pp 55–92. Springer-Verlag, Berlin.

    Google Scholar 

  • Das A and Mishra A K 1984 Aerotolerant growth inAzospirillum brasilense induced by dihydroxyphenyl iron-binding compound. Current Microbiol. 11, 313–316.

    Google Scholar 

  • Del Gallo M, Gratani L and Morpurgo G 1987 Selection at the chemostat ofAzospirillum brasilense Cd N2-fixing at high oxygen pressure.In Azospirillum IV, Genetics, Physiology, Ecology. Ed. W Klingmüller. pp. 75–82. Springer-Verlag, Berlin.

    Google Scholar 

  • Dingler Ch and Oelze J 1985 Reversible and irreversible inactivation of cellular nitrogenase upon oxygen stress inAzotobacter vinelandii growing in oxygen controlled continuous culture. Arch. Microbiol. 141, 80–84.

    PubMed  Google Scholar 

  • Elmerich C 1984 Molecular biology and ecology of diazotrophs associated with non-leguminous plants. Bio/Technology 2, 967–978.

    Google Scholar 

  • Fischer M, Levy E and Geller T 1986 Regulatory mutation that controlnif expression and histidine transport inAzospirillum brasilense. J. Bacteriol. 167, 423–426.

    PubMed  Google Scholar 

  • Fu Ch and Knowles R 1986 Oxygen tolerance of uptake hydrogenase inAzospirillum spp. Can. J. Microbiol. 32, 897–900.

    Google Scholar 

  • Gallori E and Bazzicalupo M 1985 Effect of nitrogen compounds on nitrogenase activity inAzospirillum brasilense. FEMS Microbiol. Lett. 28, 35–38.

    Google Scholar 

  • Gauthier D and Elmerich C 1977 Relationship between glutamine synthetase and nitrogenase inSpirillum lipoferum. FEMS Microbiol. Lett. 2, 101–104.

    Google Scholar 

  • Goldberg I, Nadler V and Hochman A 1987 Mechanism of nitrogenase switch-off by oxygen. J. Bacteriol. 169, 874–879.

    PubMed  Google Scholar 

  • Gordon J K and Jacobson M R 1983 Isolation and characterization ofAzotobacter vinelandii mutant strains with potential as bacterial fertilizer. Can. J. Microbiol. 29, 973–978.

    Google Scholar 

  • Gotto J W and Yoch D C 1985 Regulation of nitrogenase activity by covalent modification inChromatium vinosum. Arch. Microbiol. 141, 40–43.

    PubMed  Google Scholar 

  • Hällborn L 1984 Sarcosine: A possible regulatory compound in thePeltigera praetextata-Nostoc symbiosis. FEMS Microbiol. Lett. 22, 119–121.

    Google Scholar 

  • Halsall D M and Gibson A H 1985 Cellulose decomposition and associated nitrogen fixation by mixed cultures ofCellulomonas gelida andAzospirillum species orBacillus macerans. Appl. Environ. Microbiol. 50, 1021–1026.

    Google Scholar 

  • Halsall D M, Turner G L and Gibson A H 1985 Straw and xylan utilization by pure cultures of nitrogen-fixingAzospirillum spp. Appl. Environ. Microbiol. 49, 423–428.

    Google Scholar 

  • Hartmann A 1982 Antimetabolite effects on nitrogen metabolism ofAzospirillum and properties of resistant mutants.In Azospirillum, Genetics, Physiology, Ecology. Ed. W. Klingmüller. pp 59–68. Experientia Suppl. 42, Birkhäuser, Basel.

    Google Scholar 

  • Hartmann A 1987 Osmoregulatory properties ofAzospirillum spp.In Azospirillum IV, Genetics, Physiology, Ecology. Ed. W Klingmüller. pp. 122–130. Springer-Verlag, Berlin.

    Google Scholar 

  • Hartmann A and Burris R H 1987 Regulation of nitrogenase activity by oxygen inAzospirillum brasilense andAzospirillum lipoferum. J. Bacteriol. 169, 944–948.

    PubMed  Google Scholar 

  • Hartmann A, Fu H and Burris R H 1986 Regulation of nitrogenase activity by ammonium chloride inAzospirillum spp. J. Bacteriol. 165, 864–870.

    PubMed  Google Scholar 

  • Hartmann A, Fu H and Burris R H 1988 Influence of amino acids on nitrogen fixation ability and growth ofAzospirillum spp. Appl. Environ. Microbiol. 54, 87–93.

    PubMed  Google Scholar 

  • Hartmann A, Fu H, Song S-D and Burris R H 1985 Comparison of nitrogenase regulation inA. brasilense, A. lipoferum andA. amazonense.In Azospirillum III, Genetics, Physiology, Ecology. Ed. W Klingmüller. pp. 116–126. Springer-Verlag, Berlin.

    Google Scholar 

  • Hartmann A, Fußeder A and Klingmüller W 1983 Mutants ofAzospirillum affected in nitrogen fixation and auxin production.In Azospirillum II, Genetics, Physiology, Ecology. Ed. W Klingmüller. pp 78–88. Experientia Suppl. 48, Birkhäuser-Verlag, Basel.

    Google Scholar 

  • Hartmann A and Kleiner D 1982 Ammonium (methylammonium) transport byAzospirillum spp. FEMS Microbiol. Lett. 15, 65–67.

    Google Scholar 

  • Hartmann A, Kleiner D and Klingmüller W 1984 Ammonium uptake and release byAzospirillum.In Advances in Nitrogen Fixation Research. Eds. C Veeger and W E Newton. p. 227. Nijhoff/Junk/Pudoc Publishers, The Hague, Wageningen, The Netherlands.

    Google Scholar 

  • Heda G D and Madigan M T 1986 Aspects of nitrogen fixation inChlorobium. Arch. Microbiol. 143, 330–336.

    Google Scholar 

  • Heinrich D and Hess D 1985 Chemotactic attraction ofAzospirillum lipoferum by wheat roots and characterization of some attractants. Can. J. Microbiol. 31, 26–31.

    Google Scholar 

  • Hider R C 1984 Siderophore mediated absorption of iron. Structure Bonding 58, 26–87.

    Google Scholar 

  • Hochman A and Burris R H 1981 Effect of oxygen on acetylene reduction by photosynthetic bacteria. J. Bacteriol. 147, 492–499.

    PubMed  Google Scholar 

  • Hochman A, Goldberg I, Nadler V and Hartmann A 1987 Reversible inhibition of nitrogen fixation by oxygen.In Aspects of Nitrogen Metabolism. Eds. W R Ullrich, P J Aparicio, P J Syrett and F Castillo. pp 173–174. Springer-Verlag, Berlin.

    Google Scholar 

  • Hurek T, Reinhold B, Fendrik I and Niemann E-G 1987a Root-zone-specific oxygen tolerance ofAzospirillum spp. and diazotrophic rods closely associated with Kallar grass. Appl. Environ. Microbiol. 53, 163–169.

    Google Scholar 

  • Hurek T, Reinhold B, Niemann E-G and Fendrik I 1987b N2-dependent growth ofAzospirillum spp. in batch cultures at low concentrations of oxygen.In Azospirillum IV, Genetics, Physiology, Ecology. Ed. W Klingmüller. pp 115–121. Springer-Verlag, Berlin.

    Google Scholar 

  • Imhoff J F 1986 Osmoregulation and compatible solutes in eubacteria. FEMS Microbiol. Rev. 39, 57–66.

    Google Scholar 

  • Jouanneau Y, Meyer C M and Vignais P M 1983 Regulation of nitrogenase activity through iron protein interconversion into an active and an inactive form inRhodospeudomonas capsulata. Biochim. Biophys. Acta 749, 318–328.

    Google Scholar 

  • Kanemoto R H and Ludden P W 1984 Effect of ammonia darkness and phenazine methosulfate on whole-cell nitrogenase activity and Fe protein modification inRhodospirillum rubrum. J. Bacteriol. 158, 713–720.

    PubMed  Google Scholar 

  • Ken Dror S, Preger R and Avi-Dor Y 1986 Role of betaine in the control of respiration and osmoregulation of a halotolerant bacterium. FEMS Microbiol. Rev. 39, 115–120.

    Google Scholar 

  • Kleiner D and Castorph H 1982 Inhibition of ammonium (methylammonium) transport inKlebsiella pneumoniae by glutamine and glutamine analogues. FEBS Lett. 146, 201–203.

    PubMed  Google Scholar 

  • Kloepper J W, Leong J, Teintze M and Schroth MN 1980 Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286, 885–886.

    Google Scholar 

  • Krieg N R and Döbereiner J 1984 GenusAzospirillum.In Bergey's Manual of Systematic Bacteriology, Vol. 1 Eds. NR Krieg and J G Holt. pp. 94–104. Williams & Wilkins, Baltimore, London.

    Google Scholar 

  • Krieg N R and Hoffman P S 1986 Microaerophily and oxygen toxicity. Annu. Rev. Microbiol. 40, 107–130.

    PubMed  Google Scholar 

  • Kush A, Elmerich C and Aubert J P 1985 Nitrogenase ofSesbania Rhizobium strain ORS 571: Purification, properties and ‘switch off’ by ammonia. J. Gen. Microbiol. 131, 1765–1777.

    Google Scholar 

  • Ladha J K, Triol A C, Daroy M L, Nayak D N, Caldo G and Watanabe I 1986 Degrading straw as source of carbon and energy for nitrogen-fixing organisms in wetland rice soil. Proceedings of the Fourth International Symposium on Microbial Ecology 1986, Ljubljana (In press).

  • Leong J 1986 Siderophores: Their biochemistry and possible role in the biocontrol of plant pathogens. Annu. Rev. Phytopathol. 24, 187–209.

    Google Scholar 

  • Lowry R G, Saari L L and Ludden P W 1986 Reversible regulation of nitrogenase iron protein fromRhodospirillum rubrum by ADP-ribosylationin vitro. J. Bacteriol. 166, 513–518.

    PubMed  Google Scholar 

  • Ludden P W and Burris R H 1976 Activating factor for the iron protein of nitrogenase fromRhodospirillum rubrum. Science 194, 424–426.

    PubMed  Google Scholar 

  • Ludden P W, Okon Y and Burris R H 1978 The nitrogenase system ofSpirillum lipoferum. Biochem. J. 173, 1001–1003.

    PubMed  Google Scholar 

  • Magalhaes R M, Baldani J I, Souto SM, Kuykendall J R and Döbereiner J 1983 A new acid-tolerantAzospirillum species. An. Acad. Brasil. Cienc. 55, 417–430.

    Google Scholar 

  • Malik K A and Schlegel H G 1981 Chemolithoautotrophic growth of bacteria able to grow under N2-fixing conditions. FEMS Microbiol. Lett. 11, 63–67.

    Google Scholar 

  • Mandimba G, Heulin T, Bally R, Guckert A and Balandreau J 1986 Chemotaxis of free-living nitrogen-fixing bacteria towards maize mucilage. Plant and Soil 90, 129–139.

    Google Scholar 

  • Martinez-Drets G, Fabiano E and Cardona A 1985 Carbohydrate catabolism inAzospirillum amazonense. Appl. Environ. Microbiol. 50, 183–185.

    Google Scholar 

  • Martinez-Drets G, del Gallo M, Burpee C L and Burris R H 1984 Catabolism of carbohydrate and organic acids by the azospirilla. J. Bacteriol. 159, 80–85.

    PubMed  Google Scholar 

  • Maulik P and Ghosh S 1986 NADPH/NADH-dependent cold labile glutamate dehydrogenase ofAzospirillum brasilense. Eur. J. Biochem. 155, 595–602.

    PubMed  Google Scholar 

  • Narula N and Gupta K G 1986 Ammonia excretion byAzotobacter chroococcum in liquid culture and soil in the presence of manganese and clay minerals. Plant and Soil 93, 205–209.

    Google Scholar 

  • Nelson L M and Knowles R 1978 Effect of oxygen and nitrate on nitrogen fixation and denitrification byAzospirillum brasilense grown in continuous culture. Can. J. Microbiol. 24, 1395–1403.

    PubMed  Google Scholar 

  • Neilands J B 1984 Methodology of siderophores. Structure Bonding 58, 1–24.

    Google Scholar 

  • Neilands J B and Leong S A 1986 Siderophores in relation to plant growth and disease. Annu. Rev. Plant Physiol. 37: 187–208.

    Google Scholar 

  • Nur I, Okon Y and Henis Y 1982 Effect of dissolved oxygen tension on production of carotenoids, poly-β-hydroxybutyrate, succinate oxidase and superoxide dismutase byAzospirillum brasilense Cd grown in continuous culture. J. Gen. Microbiol. 128, 2937–2943.

    Google Scholar 

  • Nur I, Steinitz Y L, Okon Y and Henis Y 1981 Carotenoid composition and function in nitrogen-fixing bacteria of the genusAzospirillum. J. Gen. Microbiol. 122, 27–32.

    Google Scholar 

  • Okon Y 1985a The physiology ofAzospirillum in relation to its utilization as inoculum for promoting growth of plants.In Nitrogen Fixation and CO2 Metabolism. Eds. P W Ludden and J E Burris. pp. 165–174. Elsevier, New York.

    Google Scholar 

  • Okon Y 1985bAzospirillum as a potential inoculant for agriculture. Trends Biotechnol. 3, 223–228.

    Google Scholar 

  • Okon Y, Houchins J P, Albrecht S L, and Burris R H 1977 Growth ofSpirillum lipoferum at constant partial pressures of oxygen, and the properties of its nitrogenase in cell-free extracts. J. Gen. Microbiol. 98 87–93.

    PubMed  Google Scholar 

  • Okon Y and Kapulnik Y 1986 Development and function ofAzospirillum-inoculated roots. Plant and Soil 90, 3–16.

    Google Scholar 

  • Page W J and Dale P L 1986 Stimulation ofAgrobacterium tumefaciens growth byAzotobacter vinelandii ferrisiderophores. Appl. Environ. Microbiol. 51, 451–454.

    Google Scholar 

  • Patriquin D G, Döbereiner J and Jain D K 1983 Sites and process of association between diazotrophs and grasses. Can. J. Microbiol. 29, 900–915.

    Google Scholar 

  • Pedrosa F O and Yates M G 1984 Regulation of nitrogen fixation (nif) genes ofAzospirillum brasilense bynifA andntr (gln) type gene products. FEMS Microbiol. Lett. 23, 95–101.

    Google Scholar 

  • Pope M R, Murrel S A and Ludden P W 1985 Covalent modification of the iron protein of nitrogenase fromRhodospirillum rubrum by adenosine diphosphoribosylation of a specific arginyl residue. Proc. Natl. Acad. Sci. USA 82, 3173–3177.

    PubMed  Google Scholar 

  • Postgate J R 1982 The Fundamentals of Nitrogen Fixation, pp 60–102. Cambridge University Press, Cambridge.

    Google Scholar 

  • Postgate J R, Kent H M, Hill S and Blackburn H 1985 Nitrogen fixation byDesulfovibrio gigas and other species ofDesulfovibrio.In Nitrogen Fixation and CO2 Metabolism. Eds. P W Ludden and J E Burris. pp 225–234. Elsevier Science Publishers. Amsterdam.

    Google Scholar 

  • Powell P E, Cline G R, Reid C P P, and Szaniszlo P J 1980 Occurrence of hydroxamate siderophore iron chelators in soils. Nature 287, 833–834.

    Google Scholar 

  • Ramos J L and Robson R L 1985 Lesions in citrate synthase that affect aerobic nitrogen fixation byAzotobacter chroococcum. J. Bacteriol. 162, 746–751.

    PubMed  Google Scholar 

  • Rao A V and Venkateswarlu B 1985 Salt tolerance ofAzospirillum brasilense. Acta Microbiol. Hung. 32, 221–224.

    PubMed  Google Scholar 

  • Ratti S, Curti B, Zanetti G and Galli E 1985 Purification and characterization of glutamate synthase fromAzospirillum brasilense. J. Bacteriol. 163, 724–729.

    PubMed  Google Scholar 

  • Reich S, Almon H and Böger P 1986 Short-term effect of ammonia on nitrogenase activity ofAnabaena variabilis (ATCC 29413). FEMS Microbiol. Lett. 34, 53–56.

    Google Scholar 

  • Reinhold B, Hurek T and Fendrik I 1985 Strain-specific chemotaxis ofAzospirillum spp. J. Bacteriol. 162, 190–195.

    PubMed  Google Scholar 

  • Reinhold B, Hurek T, Fendrik I, Pot B, Gillis M, Kersters K, Thielemans S and De Ley J 1987Azospirillum halopraeferens sp. nov., a nitrogen-fixing organism associated with roots of Kallar grass (Leptochloa fusca (Linn.) Kunth). Int. J. Syst. Bacteriol. 37, 43–51.

    Google Scholar 

  • Robson R L and Postgate J R 1980 Oxygen and hydrogen in biological nitrogen fixation. Annu. Rev. Microbiol. 34 183–207.

    PubMed  Google Scholar 

  • Römheld V and Marschner H 1986 Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol. 80, 175–180.

    Google Scholar 

  • Saari L L, Triplett E W and Ludden P W 1984 Purification and properties of the activating enzyme for iron protein of nitrogenase from the photosynthetic bacteriumRhodospirillum rubrum. J. Biol. Chem. 259, 15502–15508.

    PubMed  Google Scholar 

  • Sampaio M J A M, Pedrosa F O and Döbereiner J 1982 Growth ofDerxia gummosa andAzospirillum spp. on C1-compounds. An. Acad. brasil. Cienc. 54, 457–458.

    Google Scholar 

  • Sandhu G R, Aslam Z, Salim M, Sattar A, Qureshi R H, Ahmad N and Wyn Jones RG 1981 The effect of salinity on the yield and composition ofDiplachne fusca (Kallar grass). Plant Cell Environ. 4, 177–181.

    Google Scholar 

  • Saxena B, Modi M and Modi V V 1986 Isolation and characterization of siderophores fromAzospirillum lipoferum D-2. J. Gen. Microbiol. 132, 2219–2224.

    Google Scholar 

  • Singh H N, Singh R K and Sharma R 1983 An L-methionine-D,L-sulfoximine-resistant mutant of the cyanobacteriumNostoc muscorum showing inhibitor-resistant δ-glutamyltransferase, defective glutamine synthetase and producing extracellular ammonia during N2-fixation. FEBS Lett. 154, 10–14.

    Google Scholar 

  • Smith M J and Neilands J B 1984 Rhizobactin, a siderophore fromRhizobium meliloti. J. Plant Nutr. 7, 449–458.

    Google Scholar 

  • Song S D, hartmann A and Burris R H 1985 Purification and properties of the nitrogenase ofAzospirillum amazonense. J. Bacteriol. 164, 1271–1277.

    PubMed  Google Scholar 

  • Spiller H, Latorre C, Hassan M E, and Shanmugam KT 1986 Isolation and characterization of nitrogenase-derepressed mutant strains of CyanobacteriumAnabaena variabilis. J. Bactriol. 165, 412–419.

    Google Scholar 

  • Stal L J and Krumbein W E 1985 Oxygen protection of nitrogenase in the aerobically nitrogen fixing, nonheterocystous cyanobacteriumOscillatoria sp. Arch. Microbiol. 143, 72–76.

    Google Scholar 

  • Sugiura Y and Nomoto K 1984 Phytosiderophores, structure and properties of mugineic acids and their metal complexes. Structure Bonding 58, 107–135.

    Google Scholar 

  • Tarrand J J, Krieg N R and Döbereiner J 1978 A taxonomic study of theSpirillum lipoferum group, with descriptions of a new genus,Azospirillum gen. nov. and two species,Azospirillum lipoferum (Beijerinck) comb. nov. andAzospirillum brasilense sp. nov. Can. J. Microbiol. 24, 967–980.

    PubMed  Google Scholar 

  • Tien T M, Diem H G, Gaskins M H and Hubbell D H 1981 Polygalacturonic acid transeliminase production byAzospirillum species. Can. J. Microbiol. 27, 426–431.

    PubMed  Google Scholar 

  • Tilak K V B R, Schneider K and Schlegel H G 1986 Autotrophic growth of nitrogen-fixingAzospirillum species and partial characterization of hydrogenase from strain CC. Current Microbiology 13, 291–297.

    Google Scholar 

  • Turpin D H, Edie S A and Canvin D T 1984In vivo nitrogenase regulation by ammonium and methylamine and the effect of MSX on ammonium transport inAnabaena flos-aguae. Plant Physiol. 74, 701–704.

    Google Scholar 

  • Volpon A G T, De-Polli H and Döbereiner J 1981 Physiology of nitrogen fixation inAzospirillum lipoferum Br 17 (ATCC 29709). Arch. Microbiol. 128, 371–375.

    Google Scholar 

  • Whiting G J, Gandy E L and Yoch D C 1986 Tight coupling of root-associated nitrogen fixation and plant photosynthesis in the salt marsh grassSpartina alterniflora and carbon dioxide enhancement of nitrogenase activity. Appl. Environ. Microbiol. 52, 108–113.

    PubMed  Google Scholar 

  • Waring W S and Werkman C H 1943 Growth of bacteria in an iron-free medium. Arch. Biochem. 1, 303–310.

    Google Scholar 

  • Whipps J M and Lynch J M 1986 The influence of the rhizosphere on crop productivity.In Advances in Microbial Ecology 9. Ed. KC Marshall. pp 187–244. Plenum Press, New York.

    Google Scholar 

  • Whipps J M and Lynch J M 1983 Substrate flow and utilization in the rhizosphere of cereals. New Phytol. 95, 605–623.

    Google Scholar 

  • Wyn Jones R G and Storey R 1981 Betaines.In Physiology and Biochemistry of Drought Resistance in Plants. Eds. L G Paleg and D Aspinall. pp 171–204. Sydney, Academic Press Australia.

    Google Scholar 

  • Yancey P H, Clark M E, Hand SC, Bowlus R D and Somero G N 1982 Living with water stress: Evolution of osmolyte systems. Science 217, 1214–1222.

    PubMed  Google Scholar 

  • Yates M G and Jones C W 1974 Respiration and nitrogen fixation inAzotobacter.In Advances in Microbial Physiology 11. Eds. AH Rose and D W Tempest. pp 97–135. Academic Press, New York.

    Google Scholar 

  • Yoch D C and Whiting G J 1986 Evidence for NH +4 switch-off regulation of nitrogenase activity by bacteria in salt marsh sediments and roots of the grassSpartina alterniflora. Appl. Environ. Microbiol. 51, 143–149.

    PubMed  Google Scholar 

  • Zuberer D A and Alexander D B 1986 Effects of oxygen partial pressure and combined nitrogen on N2-fixation (C2H2) associated withZea mays and other gramineous species. Plant and Soil 90, 47–58.

    Google Scholar 

  • Zumft W G 1985 Regulation of nitrogenase activity in the anoxygenic phototrophic bacteria.In Nitrogen Fixation Research Progress. Eds. H J Evans, P J Bottomley and W E Newton. pp 551–557. Martinus Nijhoff Publishers, Dordrecht, The Netherlands.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Lehrstuhl für Mikrobiologie, Universität Bayreuth, Postfach 101251, D-8580, Bayreuth, FRG

    A. Hartmann

Authors
  1. A. Hartmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hartmann, A. Ecophysiological aspects of growth and nitrogen fixation inAzospirillum spp.. Plant Soil 110, 225–238 (1988). https://doi.org/10.1007/BF02226803

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02226803

Key words

Search

Navigation