Skip to main content
SpringerLink
Log in

Oxygen protection of nitrogenase in the aerobically nitrogen fixing, non-heterocystous cyanobacterium Oscillatoria sp.

  • Original Papers
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Oscillatoria sp. strain 23 is a filamentous, non-heterocystous cyanobacterium that fixes nitrogen aerobically. Although, in this organism nitrogenase is inactivated by oxygen a high tolerance is observed. Up to a pO2 of 0.15 atm, oxygen does not have any measurable effects on acetylene reduction. Higher concentrations of oxygen inhibited the activity to a relatively high degree. Evidence for two mechanisms of oxygen protection of nitrogenase in this cyanobacterium was obtained. A high rate of synthesis of nitrogenase may allow the organism to maintain a certain amount of active enzyme under aerobic conditions. Secondly, a switch off/on mechanism may reversibly convert the active enzyme into a non-active form which is insensitive to oxygen inactivation after a sudden and short-term exposure to high oxygen concentrations. It is conceived that these mechanisms in addition to a temporal separation of nitrogen fixation from oxygenic photosynthesis sufficiently explain the regulation process of aerobic nitrogen fixation in this organism.

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

Abbreviations

DCMU:

3-(3,4-dichlorophenyl)-1,1-dimethylurea

CAP:

chloramphenicol

References

  • Bone DR (1971) Kinetics of synthesis of nitrogenase in batch and continuous culture of Anabaena flos-aquae. Arch Mikrobiol 80:242–251

    Google Scholar 

  • Bothe H, Loos E (1972) Effect of far red light and inhibitors on nitrogen fixation and photosynthesis in the blue-green alga Anabaena cylindrica. Arch Mikrobiol 86:241–254

    Google Scholar 

  • Cox RM (1966) Physiological studies on nitrogen fixation in the blue-green alga Anabaena cylindrica. Arch Mikrobiol 53:263–276

    Google Scholar 

  • Donze M, Haveman J, Schiereck P (1972) Absence of Photosystem II in heterocysts of the blue-green alga Anabaena. Biochim Biophys Acta 256:157–161

    Google Scholar 

  • Fay P (1969) Cell differentiation and pigment composition in Anabaena cylindrica. Arch Mikrobiol 67:62–70

    Google Scholar 

  • Fay P (1970) Photostimulation of nitrogen fixation in Anabaena cylindrica. Biochim Biophys Acta 216:353–356

    Google Scholar 

  • Fay P, Stewart WDP, Walsby AE, Fogg GE (1968) Is the heterocyst the site of nitrogen fixation in blue-green algae. Nature 220: 810–812

    Google Scholar 

  • Gallon JR, Hamadi AF (1984) Studies on the effects of oxygen on acetylene reduction (nitrogen fixation) in Gloeothece sp. ATCC 27152. J Gen Microbiol 130:495–503

    Google Scholar 

  • Gallon JR, LaRue TA, Kurz WGW (1974) Photosynthesis and nitrogenase activity in the blue-green alga Gloeocapsa. Can J Microbiol 20:1633–1637

    Google Scholar 

  • Gallon JR, Ul-Haque MI, Chaplin AE (1978) Fluoracetate metabolism in Gloeocapsa sp. LB795 and its relationship to acetylene reduction (nitrogen fixation). J Gen Microbiol 106:329–336

    Google Scholar 

  • Haaker H, Veeger C (1977) Involvement of the cytoplasmic membrane in nitrogen fixation by Azotobacter vinelandii. Eur J Biochem 77:1–10

    Google Scholar 

  • Haselkorn R (1978) Heterocysts. Ann Rev Plant Physiol 29:319–344

    Google Scholar 

  • Kallas T, Rippka R, Coursin T, Rebiere MC, Tandeau de Marsac N, Cohen-Bazire G (1983) Aerobic nitrogen fixation by non-heterocystous cyanobacteria. In: Papageorgiou GC, Packer L (eds) Photosynthetic prokaryotes. Cell differentiation and function. Elsevier, New York Amsterdam Oxford, pp 281–302

    Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randell RJ (1951) Protein measurements with Folin phenol reagent. J Biol Chem 193: 265–275

    Google Scholar 

  • Mackey EJ, Smith GD (1983) Adaptation of the cyanobacterium Anabaena cylindrica to high oxygen tensions. FEBS Lett 156:108–112

    Google Scholar 

  • McKinney G (1941) Absorption of light by chlorophyll solutions. J Biol Chem 140:315–322

    Google Scholar 

  • Mullineaux PM, Gallon JR, Chaplin AE (1981) Acetylene reduction (nitrogen fixation) by cyanobacteria grown under alternating light-dark cycles. FEMS Microbiol Lett 10:245–247

    Google Scholar 

  • Mullineaux PM, Chaplin AE, Gallon JR (1983) Synthesis of nitrogenase in the cyanobacteria Gloeothece (Gloeocapsa) sp. CCAP 1430/3. J Gen Microbiol 129:1689–1696

    Google Scholar 

  • Murry MA, Hallenbeck PC, Esteva D, Benemann JR (1983) Nitrogenase inactivation by oxygen and enzyme turnover in Anabaena cylindrica. Can J Microbiol 29:1286–1294

    Google Scholar 

  • Murry MA, Hallenbeck PC, Benemann JR (1984) Immunochemical evidence that nitrogenase is restricted to the heterocysts in Anabaena cylindrica. Arch Microbiol 137:194–199

    Google Scholar 

  • Ohmori M, Hattori A (1979) Differential effects of oxygen on N2 fixation and C2H2 reduction by Anabaena cylindrica. Plant Cell Physiol 20:1163–1166

    Google Scholar 

  • Pearson HW, Howsley R, Kjeldsen CK, Walsby AE (1979) Aerobic nitrogenase activity associated with a non-heterocystous filamentous cyanobacterium. FEMS Microbiol Lett 5:163–167

    Google Scholar 

  • Pearson HW, Malin G, Howsley R (1981) Physiological studies on in vivo nitrogenase activity by axenic cultures of the blue-green alga Microcoleus chthonoplastes. Br Phycol J 16:139

    Google Scholar 

  • Pienkos PT, Bodmer S, Tabita FR (1983) Oxygen inactivation and recovery of nitrogenase activity in cyanobacteria. J Bacteriol 153:182–190

    Google Scholar 

  • Post E, Kleiner D, Oelze J (1983) Whole cell respiration and nitrogenase activities in Azotobacter vinelandii growing in oxygen controlled continuous culture. Arch Microbiol 134:68–72

    Google Scholar 

  • Rippka R, Stanier RY (1978) The effects of anaerobiosis on nitrogenase synthesis and heterocyst development by nostocacean cyanobacteria. J Gen Microbiol 105:83–94

    Google Scholar 

  • Rippka R, Waterbury JB (1977) The synthesis of nitrogenase by non-heterocystous cyanobacteria. FEMS Microbiol Lett 2:83–86

    Google Scholar 

  • Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories, and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  • Saino T, Hattori A (1982) Aerobic nitrogen fixation by the marine non-heterocystous cyanobacterium Trichodesmium (Oscillatoria) spp.: Its protective mechanism against oxygen. Marine Biol 70:251–254

    Google Scholar 

  • Scherings G, Haaker H, Wassink H, Veeger C (1983) On the formation of an oxygen-tolerant three-component nitrogenase complex from Azotobacter vinelandii. Eur J Biochem 135:591–599

    Google Scholar 

  • Schubert W, Giani D, Rongen P, Krumbein WE, Schmidt W (1980) Photoacoustic in-vivo spectra of recent stromatolites. Naturwissenschaften 67:129–132

    Google Scholar 

  • Stal LJ, Krumbein WE (1981) Aerobic nitrogen fixation in pure cultures of a benthic marine Oscillatoria (cyanobacteria). FEMS Microbiol Lett 11:295–298

    Google Scholar 

  • Stal LJ, Krumbein WE (1985a) Nitrogenase activity in the non-heterocystous cyanobacterium Oscillatoria sp. grown under alternating light-dark cycles. Arch Microbiol 143:67–71

    Google Scholar 

  • Stal LJ, Krumbein WE (1985b) Isolation and characterization of cyanobacteria from a marine microbial mat. Bot Mar (in press)

  • Stewart WDP (1980) Some aspects of structure and functioning in N2-fixing cyanobacteria. Ann Rev Microbiol 34:497–536

    Google Scholar 

  • Stewart WDP, Lex M (1970) Nitrogenase activity in the blue-green alga Plectonema boryanum strain 594. Arch Mikrobiol 73:250–260

    Google Scholar 

  • Thomas J (1972) Relationship between age of culture and occurrence of the pigments of photosystem II of photosynthesis in heterocysts of a blue-green alga. J Bacteriol 110:92–95

    Google Scholar 

  • Weare NM, Benemann JR (1974) Nitrogenase activity and photosynthesis in Plectonema boryanum. J Bacteriol 119:258–265

    Google Scholar 

  • Wolk CP, Simon RD (1969) Pigments and lipids of heterocysts. Planta 86:92–97

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Geomicrobiology Division, University of Oldenburg, D-2900, Oldenburg, Federal Republic of Germany

    Lucas J. Stal & Wolfgang E. Krumbein

Authors
  1. Lucas J. Stal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wolfgang E. Krumbein
    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

Stal, L.J., Krumbein, W.E. Oxygen protection of nitrogenase in the aerobically nitrogen fixing, non-heterocystous cyanobacterium Oscillatoria sp.. Arch. Microbiol. 143, 72–76 (1985). https://doi.org/10.1007/BF00414771

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00414771

Key words

Search

Navigation