Marine Nitrogen-Fixing Diatom-Cyanobacteria Symbioses

  • Tracy A. Villareal
Part of the NATO ASI Series book series (ASIC, volume 362)


This review summarizes growth and nitrogen-fixation data on diatom-cyanobacteria symbioses. Symbiotic associations between diatoms and filamentous cyanobacteria are frequently noted in tropical and subtropical waters, and direct evidence indicates that at least two associations are diazotrophic. Abundance data is limited, but Rhizosolenia-Richelia blooms are recorded from the central Pacific gyre at up to 104 cells L−1. In-situ growth rates of these associations are not known; however, laboratory data on the Rhizosolenia-Richelia symbiosis suggests the host-symbiont association can reproduce at approximately 0.8–1.0 div day−1. Growth kinetics in nitrogen-poor medium suggest that transfer of fixed nitrogen from host to symbiont occurs and that this process can support the host’s growth under N-limiting conditions. Additional symbioses, particularly in Hemiaulus, may be more widespread than previously realized due to the difficulty in identifying the symbiont in standard light microscopy. Few field measurements of N2-fixation are available for these associations. Rhizosolenia-Richelia appears to be locally important in the central Pacific gyre. Hemiaulus spp. are a common and abundant diatom in oligotrophic seas, and if 80–100% of the cells are symbiotic as reported, then they represent an unquantified, and potentially substantial, source of nitrogen-fixation.


Nitrogen Fixation Acetylene Reduction Deep Chlorophyll Maximum Woods Hole Oceanographic Institution Heterocystous Cyanobacterium 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Carpenter, E.J. (1983) ‘Physiology and ecology of marine planktonic Oscillatoria (Trichodesmium)’, Mar. Biol. Lett., 4, 69–85.Google Scholar
  2. Deyoe, H. R. (1991) ‘Preliminary characterization of the relationship between Rhopalodia gibba (Bacillariophyceae) and its cyanobacterial endosymbiont’, Ph.D dissertation, Bowling Green State University, Bowling Green, 73 pp.Google Scholar
  3. Drouet, F. (1973), Revision of the Nostocaeae with Cylindrical Trichomes, Hafner Press, New York, pp. 292.Google Scholar
  4. Duce, R.A. (1986) ‘The impact of atmospheric nitrogen, phosphorus, and iron species on marine biological productivity’, in P. Buat-Menard (eds.), The Role of Air-Sea Exchange in Geochemical Cycling, D. Reidel Publ. Co., Dordrecht, Holland, pp. 497–529.CrossRefGoogle Scholar
  5. Floener, L. and Bothe, H. (1980) ‘Nitrogen fixation in Rhopalodia gibba, a diatom containing blue-greenish inclusions symbiotically’, in W. Schwemmler and H. E. A. Schenk (eds.), Endocytobiology, Endosymbiosis and Cell Biology, Walter de Gruyter & Co., New York, pp. 541–552.Google Scholar
  6. Fogg, G.E. (1982) ‘Marine plankton’, in N. G. Carr and B. A. Whitton (eds.), The Biology Cyanobacteria, University of California Press, Berkeley, pp. 491–513.Google Scholar
  7. Geitler, L. (1977) ‘Zur Entwicklungsgeschichte der Epithemiaceen Epithemia, Rhopalodia un Denticula (Diatomophyceae) un ihre vermutlich symbiontischen Sphäroidkörper. Plant Syst. Evol. 128, 259–275.CrossRefGoogle Scholar
  8. Guillard, R.R.L. and Kilham, P. (1977) ‘The ecology of marine planktonic diatoms’, in D. Werner (eds.), The Biology of Diatoms, University of California Press, Berkeley, pp. 372–46.Google Scholar
  9. Hallegraeff, G.M. and Jeffery, S.W. (1984) ‘Tropical phytoplankton species and pigments of continental shelf waters of North and North-west Australia’, Mar. Ecol. Prog. Ser., 20, 59–74.CrossRefGoogle Scholar
  10. Hawser, S.P, Codd, G. A., Capone, D. G., and Carpenter, E.J. (1991) A neurotoxic factor associated with the bloom-forming cyanobacterium Trichodesmium. Toxicon, 29, 277–278.PubMedCrossRefGoogle Scholar
  11. Heinbokel, J.F. (1986) ‘Occurrence of Richelia intracellularis (Cyanophyta) within the diatoms Hemiaulus haukii and H. membranaceus off Hawaii’, J. Phycol., 22, 399–403.CrossRefGoogle Scholar
  12. Hustedt, F. (1930) ‘Die Kieselalgen Deutschlands, Österreichs und der Schweiz met Berücksichtigung der übrigen Länder Europas sowie der anschliessenden Meeresgebiete’, in R. L. (eds.), Kryptogamenflora von Deutschlands, Österreichs und der Schweiz, Akad. Verlagsgesellschaft, Leipzig, pp. 1–920.Google Scholar
  13. Karsten G. (1905) ‘Das phytoplankton des atlantischen oceans nach dem material der deutschen Tiefsee-Expedition 1898-1899’. Wissen. Erg. Deut. Tiefsee-Exped. “VALDIVA” 1898–1899, 2, 137–219.Google Scholar
  14. Karsten, G. (1907) ‘Das indische Phytoplankton nach dem Material der deutschen Tiefsee-Expedition 1898–1899’, Wissen. Erg. Deut. Tiefsee-Exped. “VALDIVA” 1898-1899, 2: 221–548.Google Scholar
  15. Kimor, B., Reid, F.M.H. and Jordan, J.B. (1978) ‘An unusual occurrence of Hemiaulus membranaceus Cleve (Bacillariophyceae) with Richelia intracellularis Schmidt (Cyanophyceae) off the coast of Southern California in October 1976’, Phycol., 17, 162–166.CrossRefGoogle Scholar
  16. Kromkamp, J. (1991) Buoyancy regulation and vertical distribution in Trichodesmium. This Volume.Google Scholar
  17. Lemmermann, E. (1905) ‘Die Algenflora der Sandwich-Inseln. Ergebnisse einer Reise nach dem Pacific, H. Schauinsland 1896/97’, Engler’s Bot. Jb., 34, 607–663.Google Scholar
  18. Mague, T.H., Mague, F.C. and O. Holm-Hansen (1977) ‘Physiology and chemical composition of nitrogen-fixing phytoplankton in the central North Pacific Ocean’, Mar. Biol., 41, 213–227.CrossRefGoogle Scholar
  19. Mague, T.H., Weare, N.M. and Holm-Hansen, O. (1974) ‘Nitrogen fixation in the North Pacific Ocean’, Mar. Biol, 24, 109–119.CrossRefGoogle Scholar
  20. Marshall, H. G. (1981) ‘Occurrence of bluegreen algae (Cyanophyta) in the phytoplankton off the southeastern coast of the United States’, J. Plankt. Res., 3, 163–166.CrossRefGoogle Scholar
  21. Marshall, H.G. (1982) ‘Phytoplankton distribution along the eastern coast of the USA IV. Shelf waters between Cape Lookout, North Carolina, and Cape Canaveral, Florida’, Proc. Biol. Soc. Wash., 95, 99–113.Google Scholar
  22. Martinez, L., Silver, M.W., King, J.M., and Alldredge, A.L. (1983) ‘Nitrogen fixation by floating diatom mats: a source of new nitrogen to oligotrophic ocean waters’, Science, 221:152–154.PubMedCrossRefGoogle Scholar
  23. Marumo, R. and Asaoka, 0. (1974) ‘Distribution of pelagic blue-green alagae in the North Pacific Ocean’, J. Oceanogr. Soc. Jap., 30, 77–85.CrossRefGoogle Scholar
  24. Noms, R.E. (1961) ‘Observations on phytoplankton organisms collected on the N.Z.O.I. Pacific cruise, September 1958’, N.Z. J. Sci., 4, 162–188.Google Scholar
  25. Norris, R.E. (1967) ‘Algal consortisms in marine plankton’, in V. Krishnamurthy (eds.), Proc. Seminar on Sea, Salt and Plants, 1965, Catholic Press, Ranchi (Bihar), India, Central Salt and Marine Chemicals Research Institute, Bhavnagar, India, pp. 178–189.Google Scholar
  26. Ostenfeld, C.H. and Schmidt, J. (1901) ‘Plankton fra det Rode hav og Adenbugten’, Vidensk. Meddel. Naturh. Forening i Kbhvn., 141-182.Google Scholar
  27. Paasche, E. (1980) ‘Silicon’, in I. Morris (eds.), The Physiological Ecology of Phytoplankton, Blackwell Scientific Publications, Boston, pp. 259–284.Google Scholar
  28. Peters, G.A. (1978) ‘Blue-green algae and algal associations’, BioScience, 28, 580–585.CrossRefGoogle Scholar
  29. Rueter, J.G. (1988) ‘Iron stimulation of photosynthesis and nitrogen fixation in Anabaena 7120 and Trichodesmium (Cyanophyta)’, J. Phycol., 24, 249–254.Google Scholar
  30. Rueter, J.G. and Petersen, R.R. (1987) ‘Micronutrient effects on cyanobacterial growth and physiology’, N. Z. Jour. Mar. Fresh. Res., 21, 435–445.CrossRefGoogle Scholar
  31. Saino, T. (1977) Nitrogen fixation in the ocean with emphasis on the nitrogen-fixing blue-green alga Trichodesmium and its significance in the nitrogen cycling in the low latitude sea areas. Ph.D. dissertation, University of Toyko, 153 pp.Google Scholar
  32. Saunders, R. P. and Glen, D. A. (1969) ‘Diatoms.’ Mem. Hourglass Cruises I,. Fla. Dept. Nat. Resources Mar. Res. Lab., St. Petersburg, p. 1–119.Google Scholar
  33. Smith, D.C. and Douglas, A.E. (1987), The Biology of Symbiosis, Edward Arnold, Baltimore, pp. 302.Google Scholar
  34. Sournia, A. (1970) ‘Les cyanophycees dans le plancton marin’, Ann. Biol., 9, 63–76.Google Scholar
  35. Stewart, W.D.P., Rowell, P. and Rai, A.N. (1983) ‘Cyanobacterial-eukaryotic plant symbioses’, Ann. Microbiol. (Inst. Pasteur), 134 B, 205–228.CrossRefGoogle Scholar
  36. Sundström, B.G. (1984) ‘Observations on Rhizosolenia clevei Ostenfeld (Bacillariophyceae) and Richelia intracellularis Schmidt’, Bot. Mar, 27, 345–355.CrossRefGoogle Scholar
  37. Taylor, D.L. (1983) ‘Symbioses’, in E. J. Carpenter and D. G. Capone (eds.), Nitrogen in the Marine Environment, Academic Press, New York, pp. 679–697.Google Scholar
  38. Taylor, F.J.R. (1982) ‘Symbioses in marine microplankton’, Ann. Inst. Océanogr., Paris, 58 S, 61–90.Google Scholar
  39. Venrick, E. L. (1974). ‘The distribution and significance of Richelia intracellularis Schmidt in the North Pacific Central Gyre’, Limnol. Oceanogr. 19, 437–445.CrossRefGoogle Scholar
  40. Villareal, T.A. (1989) ‘Division cycles in the nitrogen-fixing Rhizosolenia (Bacillariophyceae)-Richelia (Nostocaceae) symbiosis’, Br. Phycol. J, 24, 357–365.CrossRefGoogle Scholar
  41. Villareal, T.A. (1990) ‘Laboratory cultivation and preliminary characterization of the Rhizosolenia (Bacillariophyceae)-Richelia (Cyanophyceae) symbiosis’, P.Z.S.N. I: Mar. Ecol., 11, 117–132.CrossRefGoogle Scholar
  42. Villareal, T.A. (in press) ‘Nitrogen-fixation by the cyanobacterial symbiont of the diatom genus Hemiaulus’, Mar. Ecol. Progr. Ser.Google Scholar
  43. Villareal, T.A. and Carpenter, E.J. (1989) ‘Nitrogen-fixation, suspension characteristics and chemical composition of Rhizosolenia mats in the central North Pacific Gyre’, Biol. Oceanogr., 6, 387–405.Google Scholar
  44. Villareal, T.A. and Carpenter, E.J. (1990) ‘Diel buoyancy regulation in the marine diazotrophic cyanobacterium Trichodesmium thiebautii Ehr.’, Limnol. Oceanogr., 35, 1832–1837.CrossRefGoogle Scholar
  45. Villareal, T. A. (in press) ‘Nitrogen fixation by the cyanobacterial symbiont of the diatom genus Hemiaulus’, Mar. Ecol. Prog. Ser.Google Scholar
  46. Walsby, A.F. (1978) ‘The properties and buoyancy-providing role of gas vacuoles in Trichodesmium Ehrenberg’, Br. Phycol. J., 13, 103–116.CrossRefGoogle Scholar
  47. Weare, N.M., Azam, F., Mague, T.H. and Holm-Hansen, O. (1974) ‘Microautoradiograhic studies of the marine phycobionts Rhizosolenia and Richelia’, J. Phycol., 10, 369–371.Google Scholar
  48. Wood, E.J.F. (1965) Marine Microbial Ecology, New York, Reihhold, 243 pp.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 1992

Authors and Affiliations

  • Tracy A. Villareal
    • 1
  1. 1.Woods Hole Oceanographic InstitutionWoods HoleUSA

Personalised recommendations