Abstract
The aerobic nitrogen-fixing cyanobacterium, Cyanothece sp. BH68K produces non-mucoid variants defective in exopolysaccharide (EPS) production at a high frequency. The EPS-producing wild-type colonies (EPS+) have a characteristic smooth and shiny appearance which allows them to be easily distinguished from the EPS- variants. When grown on agar plates lacking a source of combined nitrogen, the EPS- variants exhibited a yellow phenotype typical of nitrogen starvation. These EPS- variants showed varying degrees of reversion back to the EPS+ phenotype. After reversion, they exhibited normal diazotrophic growth on agar plates. Alcian blue and ruthenium red staining indicated that the EPS is an acidic polysaccharide, which is present as a loose network around the cell, and which can be completely removed by low speed centrifugation. The accumulation of EPS takes place mainly during the stationary phase. All EPS- variants failed to produce any EPS. Analysis of growth of wild-type and EPS- variants revealed that EPS production is beneficial for diazotrophic growth on solid medium, but not in liquid medium. In addition, EPS phenotypic alteration may have some advantage in the dispersal of cells from one place to another in the natural environment.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bar-Or, Y., Kessel, M., & Shilo, M. 1988 Mechanisms for release of the benthic cyanobacterium Phormidium strain J-1 to the water column. In Microbial Mats; Physiological Ecology of Benthic Microbial Communities, eds Cohen, Y., & Rosenberg, E. pp. 214–218. Washington, D.C.: American Society for Microbiology.
Bartlett, D.H., Wright, M.E., & Silverman, M. 1988 Variable expression of extracellular polysaccharide in the marine bacterium Pseudomonas atlantica is controlled by genome rearrangement. Proceedings of the National Academy of Sciences of the United States of America 85, 3923–3927.
Bertocchi, C., Navarini, L., & Cesaro, A. 1990 Polysaccharides from cyanobacteria. Carbohydrate Polymers 12, 127–153.
Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., & Smith, F. 1956 Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28, 350–356.
Gallon, J.R. 1992 Reconciling the incompatable: N2 fixation and O2. New Phytologist 122, 571–609.
Grossman, A.R., Schaefer, M.R., Chiang, G.G., & Collier, J.L. 1993 Environmental effects on the light-harvesting complex of Cyanobacteria. Journal of Bacteriology 175, 575–582.
Huang, T.C., & Grobbelaar, N. 1995 The circadian clock in the prokaryote. Synechococcus RF-1. Microbiology 141, 535–540.
Kallas, T., Rippka, R., Coursin, T., Rebiere, M., Tandau de Marsac, N. & Cohen-Bazire, G. 1983 Aerobic nitrogen fixation by non-heterocystous cyanobacteria. In Photosynthetic Procaryotes, Cell Differentiation and Function, eds Papageorgiu, G., & Packer, L. pp. 281–302. New York: Elsevier.
Maynard, R.H., Premkumar, R., & Bishop, P.E. 1994 Mo-Independent nitrogenase 3 is advantageous for diazotrophic growth of Azotobacter vinelandi on solid medium containing molybdenum. Journal of Bacteriology 176, 5583–5586.
Mitsui, A., Kumazawa, S., Talahashi, A., Ikemoto, H., Cao, S., & Arai, T. 1986 Strategy by which nitrogen-fixing unicellular cyanobacteria grow photoautotrophically. Nature 323, 720–722.
Mutaftschiev, S., Vasse, J., & Truchet, G. 1982 Exostructures of Rhizobium meliloti. FEMS Microbiology Letters 13, 171–175.
Panoff, J.M., Priem, B., Morvan, H., & Joset, F. 1988 Sulphated exopolysaccharides produced by two unicellular strains of cyanobacteria, Synechococcus PCC6803 and 6714. Archives of Microbiology 150, 558–563.
Perkins, F.O., Haas, L.W., Phillips, D.E., & Webb, K.L. 1981 Ultrastructure of a marine Synechococcus possessing spinae. Canadian Journal of Microbiology 27, 318–329.
Philippis, R.D., Margheri, M.C., Pelosi, E., & Ventura, S. 1993 Exopolysaccharide production by a unicellular cyanobacterium isolated from a hypersaline habitat. Journal of Applied Phycology 5, 387–394.
Phlips, E.J., Zeman, C., & Hansen, P. 1989 Growth, photosynthesis, nitrogen fixation and carbohydrate production by a unicellular cyanobacterium, Synechocystis sp. (Cyanophyta). Journal of Applied Phycology 1, 137–145.
Prosperi, C.H. 1994 A cyanophyte capable of fixing nitrogen under high levels of oxygen. Journal of Phycology 30, 222–224.
Rainey, P.B., Moxon, E.R., & Thompson, I.P. 1993 Intraclonal polymorphism in bacteria. Advances in Microbial Ecology 13, 263–300.
Reddy, K.J., Haskell, J.B., Sherman, D.M., & Sherman, L.A. 1993 Unicellular aerobic nitrogen-fixing cyanobacteria of the genus Cyanothece. Journal of Bacteriology 175, 1284–1292.
Reimels, A.J., & Reddy, K.J. 1995 Analysis of Cyanothece sp. BH68K mutants defective in aerobic nitrogen fixation. Current Microbiology 31, 174–179.
Rippka, R., Deruelles, J., Waterbury, J.B., Herdman, M., & Stanier, R.Y. 1979 Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Journal of General Microbiology 111, 1–61.
Salhi, B., & Mendelson, N.H. 1993 Patterns of gene expression in Bacillus subtilis colonies. Journal of Bacteriology 175, 5000–5008.
Sandford, P.A. 1985 Applications of marine polysaccharides in the chemical industry. In Biotechnology in the Marine Sciences: Biotechnology of Marine Polysaccharides, eds Colwell, R.R., Pariser, E.R. & Sinskey, A.J. pp. 451–516. New York: McGraw-Hill.
Schneegurt, M.A., Sherman, D.M., Nayer, S., & Sherman, L.A. 1994 Oscillating behavior of carbohydrate granule formation and dinitrogen fixation in the cyanobacterium Cyanothece sp. strain ATCC51142. Journal of Bacteriology 176, 1586–1597.
Shapiro, J.A., & Higgins, N.P. 1988 Variation of β-galactosidase expression from MUdlac elements during development of Escherichia coli colonies. Annals of the Institute Pasteur/Microbiology 139, 70–103.
Silverman, M., & Simon, M. 1983 Phase variation and related systems. In Mobile Genetic Elements, ed Shapiro, J.A. pp. 537–557 New York: Academic Press.
Soper, B.W., & Reddy, K.J. 1994 Identification of a nuclease and host restriction-modification in the unicellular, aerobic nitrogen-fixing cyanobacterium, Cyanothece sp. Journal of Bacteriology 176, 5565–5570.
Soper, B.W., & Reddy, K.J. 1995 Distribution and homology of plasmids in several strains of Cyanothece. Current Microbiology 31, 169–173.
Sudo, H., Burgess, J.G., Takemasa, H., Nakamura, N., & Matsunaga, T. 1995 Sulphated exopolysaccharide production by the halophilic cyanobacterium Aphanocapsa halophytica. Current Microbiology 30, 219–222.
Sutherland, I.W. 1988 Bacterial surface polysaccharides: structure and function. International Review of Cytology 113, 187–231.
Vaara, T. 1982 The outermost surface structures in chroococcacean cyanobacteria. Canadian Journal of Microbiology 28, 929–941.
Vincenzini, M., De Philippis, R., Sili, C., & Materassi, R. 1990 A novel exopolysaccharide from a filamentous cyanobacterium: production, chemical characterization and rheological properties. In Novel Biodegradable Microbial Polymers, ed Dawes, E.A. pp. 295–310. Dordrecht: Kluwer Academic Publishers.
Whitfield, C. 1988 Bacterial extracellular polysaccharides. Canadian Journal of Microbiology 34, 415–420.
Additional information
K.J. Reddy. J. Tang and R.L. Bradley are, and B.W. Soper was, with the Department of Biological Sciences, State University of New York at Binghamton, Binghamton, NY 13902; B.W. Soper is now with the Jackson Laboratory, Box 302, 600 Main St., Bar Harbor, ME 04609.
Rights and permissions
About this article
Cite this article
Reddy, K.J., Soper, B.W., Tang, J. et al. Phenotypic variation in exopolysaccharide production in the marine, aerobic nitrogen-fixing unicellular cyanobacterium Cyanothece sp.. World Journal of Microbiology & Biotechnology 12, 311–318 (1996). https://doi.org/10.1007/BF00340206
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00340206