Archives of Microbiology

, Volume 145, Issue 3, pp 259–265 | Cite as

Growth characteristics of non-heterocystous cyanobacterium Plectonema boryanum with N2 as nitrogen source

  • Dieter Giani
  • Wolfgang E. Krumbein
Original Papers
Received:
Accepted:

Abstract

Strains of filamentous, non-heterocystous cyanobacteria from the Pasteur Culture Collection (PCC), able to synthesize nitrogenase under anaerobic test conditions, were tested for growth with N2 as sole nitrogen source at low O2 partial pressure (less than 0.05%).

Plectonema boryanum (PCC 73110) exhibited exponential growth under these conditions. This capacity was restricted to light intensities not exceeding 500 lux. Growth rates were 0.014/h at 200 and 0.023 at 500 lux and similar to those of anaerobic and aerobic control cultures with nitrate as N-source. For N2-fixing cultures incubated at 200 and 500 lux, acetylene reduction rates were 4–8 and 5–14 nmol C2H4 per mg protein per min, respectively. The ratio of phycocyanine to chlorophyll was higher (200 lux) or slightly reduced (500 lux) in N2-fixing cultures as compared to control cultures with nitrate as N-source. On the basis of epifluorescence microscopy and microfluorimetry, no differences in pigment contents were found between individual cells or filaments of N2-fixing cultures. Also no noteworthy differences were observed between the pycobiliprotein composition of individual cells in N2 fixing cultures as compared to nitrate-grown controls. Thus the observed exponential growth of P. boryanum at low light intensities implies simultaneous nitrogen fixation and oxygenic photosynthesis. Additional continuous culture experiments showed that N2-fixing exponential growth was dependent on O2 partial pressures lower than 0.2–0.4%.

The other strains tested (PCC 6412, 6602, 7403, 7104) did not grow under such conditions.

Key words

Plectonema boryanum N2-fixation Exponential growth Microaerobiosis Light Pigments 

Abbreviations

Chl

chlorophyll

PBP

phycobiliproteins

PC

phycocyanin

PCC

Pasteur Culture Collection

OD

optical density

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References

  1. Allen MM, Smith AJ (1969) Nitrogen chlorosis in blue-green algae. Arch Mikrobiol 69:114–120Google Scholar
  2. Burns RC, Hardy RWF (1975) Nitrogen fixation in bacteria and higher plants. Springer, BerlinGoogle Scholar
  3. Cohen Y (1984) The Solar Lake cyanobacterial mats: Strategies of life under sulfide. In: Cohen Y, Castenholz RW, Halvorson HO (eds) Microbial mats: Stromatolites. Allen Liss, New YorkGoogle Scholar
  4. Gallon JR (1980) Nitrogen fixation by photoautotrophs. In: Stewart WDP, Gallon JR (eds) Proceedings of an International Symposium on Nitrogen Fixation. Academic Press, London, pp 197–238Google Scholar
  5. Garlick S, Oren A, Padan E (1977) Occurrence of facultative anoxygenic photosynthesis among filamentous and unicellular cyanobacteria. J Bact 129:623–629Google Scholar
  6. Giani D, Krumbein WE (1982) N2-fixation in non-heterocystous cyanobacteria: Plectonema boryanum. Zlb Bakt Mikrobiol Hyg, I Abt Orig C 3:537Google Scholar
  7. Giani D (1983) N2-Fixierung bei Plectonema boryanum und anderen Cyanobakterien ohne Heterocysten. Dissertation, Universität OldenburgGoogle Scholar
  8. Harnischfeger G, Codd GA (1978) Factors affecting energy transfer from phycobilisomes to thylakoids in Anacystis nidulans. Biochim Biophys Acta 502:507–513Google Scholar
  9. Kalininskaya TA, Pankratova EM, Khokhlova VF (1981) Assimilation of molecular nitrogen by cyanobacteria that do not form heterocysts. Mikrobiologiya 50:550–555Google Scholar
  10. Kallas T, Rippka R, Coursin T, Rebiere MC, Tandeau de Marsac N, Cohen-Bazire G (1983) Aerobic nitrogen fixation by nonheterocystous cyanobacteria. In: Papageorgiou GC, Packer L (eds) Photosynthetic prokaryotes. Elsevier, Amsterdam, pp 281–302Google Scholar
  11. Katoh T, Ohki K (1975) Loss of photosystem II induced by nitrate deficiency in photoorganotrophically grown Anabaena varibilis. Plant Cell Physiol 16:815–828Google Scholar
  12. Katoh T, Ohki K (1976) Regeneration of photosystem II and phycobilin pigments in photoorganotrophically grown Anabaena variabilis. Plant Cell Physiol 17:525–536Google Scholar
  13. Kenyon CN, Rippka R, Stanier RY (1972) Fatty acid composition and physiological properties of some filamentous blue-green algae. Arch Mikrobiol 83:216–236Google Scholar
  14. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–276Google Scholar
  15. Meeks JC, Wolk CP, Lockau W, Schilling N, Schaffer PW, Chin WS (1978) Pathways of assimilation of (13N)N2 and (13N)NH4+ by cyanobacteria with and without heterocysts. J Bact 134:125–130Google Scholar
  16. Nickerson WJ, Strauss PW (1960) The photochemical cleavage of water by riboflavine. J Am Chem Soc 82:5007–5008Google Scholar
  17. Padan E (1979) Impact of facultative anaerobic photoautotrophic metabolism on ecology of cyanobacteria (blue-green algae). Adv Microbial Ecol 3:1–48Google Scholar
  18. Pearson HW, Howsley R (1980) Concomitant photoautotrophic growth and nitrogenase activity by cyanobacterium Plectonema boryanum in continuous culture. Nature 288:263–265Google Scholar
  19. Pearson HW, Howsley HR, Kjeldsen CK, Walsby AE (1979) Aerobic nitrogenase activity associated with a nonheterocystous filamentous cyanobacterium. FEMS Microbiol Lett 5:163–167Google Scholar
  20. Pearson HW, Malin G, Howsley R (1981) Physiological study on in vitro nitrogenase activity by axenic cultures of the blue green alga Microcoleus chthonoplastes. Brit Phycol J 16:139Google Scholar
  21. Peterson RB, Dolan E, Calvert HE, Ke B (1981) Energy transfer from phycobiliproteins to photosystem I in vegetative cells and heterocysts of Anabaena variabilis. Biochim Biophys Acta 634:237–248Google Scholar
  22. Rippka R, Waterbury JB (1977) The synthesis of nitrogenase by non-heterocystous cyanobacteria. FEMS Microbiol Lett 2:83–86Google Scholar
  23. Rippka R, Neilson A, Kunisawa R, Cohen-Bazire G (1971) Nitrogen fixation by unicellular blue-green algae. Arch Mikrobiol 76:241–348Google Scholar
  24. 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 111:1–61Google Scholar
  25. Rogerson AC (1980) Nitrogen-fixing growth by non-heterocystous cyanobacterium Plectonema boryanum. Nature 284:563–564Google Scholar
  26. Stal LJ, Krumbein WE (1981) Aerobic nitrogen fixation in pure cultures of a benthic marine Oscillatoria (cyanobacteria). FEMS Microbiol Lett 11:295–298Google Scholar
  27. Stal LJ, Krumbein WE (1985) Nitrogenase activity in the nonheterocystous cyanobacterium Oscillatoria sp. grown under alternating light-dark cycles. Arch Microbiol 143:67–71Google Scholar
  28. Stanier RY (1977) The position of the cyanobacteria in the world of phototrophs. Carlsberg Res Commun 42:77–98Google Scholar
  29. Stewart WDP, Lex M (1970) Nitrogenase activity in the blue-green alga Plectonema boryanum strain 594. Arch Mikrobiol 73:250–260Google Scholar
  30. Stewart WDP, Mague T, Fitzgerald GP (1971) Nitrogenase activity in Wisconsin lakes of different degrees of eutrophication. New Phytologist 70:497–509Google Scholar
  31. Susor WA, Krogmann DW (1964) Hill activity in cell-free preparations of a blue-green alga. Biochim Biophys Acta 88:11–19Google Scholar
  32. Van Gorkum HJ, Donze M (1971) Localisation of nitrogen fixation in Anabaena. Nature 234:231–232Google Scholar
  33. Van Liere L, Walsby AE (1982) Interactions of cyanobacteria with light. In: Carr NG, Whitton BA (eds) The biology of cyanobacteria. Blackwell Scientific Publications, Oxford, pp 9–46Google Scholar
  34. Weare NM, Benemann JR (1974) Nitrogenase activity and photosynthesis in Plectonema boryanum. J Bacteriol 119:258–265Google Scholar

Copyright information

© Springer-Verlag 1986

Authors and Affiliations

  • Dieter Giani
    • 1
  • Wolfgang E. Krumbein
    • 1
  1. 1.Geomicrobiology DivisionUniversity of OldenburgOldenburgFederal Republic of Germany

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