1887

Abstract

In the presence of ammonium ion, strain AV1, a filamentous, heterocystous cyanobacterium isolated from the Baltic Sea, lost aerobic nitrogen-fixation activity while maintaining heterocyst frequency along the filaments. Real-time RT-PCR showed that the expression of (encoding the dinitrogenase reductase component of the nitrogenase enzyme) was suppressed and the levels of NifH protein decreased dramatically in response to treatment with ammonium. On the other hand, (encoding the global nitrogen regulator in cyanobacteria) and (the key regulatory gene in heterocyst differentiation) were expressed and their expression patterns were not affected by the treatment with ammonium. These data demonstrate that strain AV1 maintains heterocyst frequency along the filaments in the presence of ammonium and in the absence of detectable N-fixation activity.

Keyword(s): Chl a, chlorophyll a
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/007849-0
2007-11-01
2019-10-15
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/11/3704.html?itemId=/content/journal/micro/10.1099/mic.0.2007/007849-0&mimeType=html&fmt=ahah

References

  1. Adams, D. G. & Duggan, P. S. ( 1999; ). Tansley Review no. 107. Heterocyst and akinete differentiation in cyanobacteria. New Phytol 144, 3–33.[CrossRef]
    [Google Scholar]
  2. Black, T. A., Cai, Y. P. & Wolk, C. P. ( 1993; ). Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena. Mol Microbiol 9, 77–84.[CrossRef]
    [Google Scholar]
  3. Bonsdorff, E., Ronnberg, C. & Aarnio, K. ( 2002; ). Some ecological properties in relation to eutrophication in the Baltic Sea. Hydrobiologia 475, 371–377.
    [Google Scholar]
  4. Bothe, H. ( 1982; ). Nitrogen fixation. In The Biology of Cyanobacteria, pp. 87–104. Edited by N. G. Carr & B. A. Whitton. Oxford: Blackwell Scientific Publications.
  5. Bottomley, P. J., Grillo, J. F., Van Baalen, C. & Tabita, F. R. ( 1979; ). Synthesis of nitrogenase and heterocysts by Anabaena sp. CA in the presence of high levels of ammonia. J Bacteriol 140, 938–943.
    [Google Scholar]
  6. Braun-Howland, E. B., Lindblad, P., Nierzwicki-Bauer, S. A. & Bergman, B. ( 1988; ). Dinitrogenase reductase (Fe-protein) of nitrogenase in the cyanobacterial symbionts of three Azolla species: localization and sequence of appearance during heterocyst differentiation. Planta 176, 319–332.[CrossRef]
    [Google Scholar]
  7. Buikema, W. J. & Haselkorn, R. ( 1991; ). Characterization of a gene controlling heterocyst differentiation in the cyanobacterium Anabaena 7120. Genes Dev 5, 321–330.[CrossRef]
    [Google Scholar]
  8. Capone, D. G. ( 1993; ). Determination of nitrogenase activity in aquatic samples using the acethylene reduction procedure. In Handbook of Methods in Aquatic Microbial Ecology, pp. 621–631. Edited by P. Kemp, B. F. Sherr, E. B. Sherr & J. J. Cole. Boca Raton, FL: Lewis Publishers.
  9. Dong, Y., Huang, X., Wu, X. Y. & Zhao, J. ( 2000; ). Identification of the active site of HetR protease and its requirement for heterocyst differentiation in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 182, 1575–1579.[CrossRef]
    [Google Scholar]
  10. Eaton, A. D., Clesceri, L. S. & Greenberg, A. E. ( 1995a; ). Phenate method. In Standard Methods for the Examination of Water and Wastewater, pp. 4.80–4.81. Washington, DC: American Public Health Association.
  11. Eaton, A. D., Clesceri, L. S. & Greenberg, A. E. ( 1995b; ). Ultraviolet spectrophotometric screening method. In Standard Methods for the Examination of Water and Wastewater, pp. 4.85–4.86. Washington, DC: American Public Health Association.
  12. Ehira, S. & Ohmori, M. ( 2006; ). NrrA directly regulates expression of hetR during heterocyst differentiation in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 188, 8520–8525.[CrossRef]
    [Google Scholar]
  13. El-Shehawy, R., Lugomela, C., Ernst, A. & Bergman, B. ( 2003; ). Diurnal expression of hetR and diazocyte development in the filamentous non-heterocystous cyanobacterium Trichodesmium erythraeum. Microbiology 149, 1139–1146.[CrossRef]
    [Google Scholar]
  14. Enell, M. & Fejes, J. ( 1995; ). The nitrogen load to the Baltic Sea – present situation, acceptable future load and suggested source reduction. Water Air Soil Pollut 85, 877–882.[CrossRef]
    [Google Scholar]
  15. Fay, P. ( 1992; ). Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Rev 56, 340–373.
    [Google Scholar]
  16. Flores, E. & Herrero, A. ( 1994; ). Assimilatory nitrogen metabolism and its regulation. In The Molecular Biology of Cyanobacteria, pp. 487–517. Edited by D. A. Bryant. Dordrecht: Kluwer.
  17. Flores, E. & Herrero, A. ( 2005; ). Nitrogen assimilation and nitrogen control in cyanobacteria. Biochem Soc Trans 33, 164–167.[CrossRef]
    [Google Scholar]
  18. Flores, E., Frias, J. E., Rubio, L. M. & Herrero, A. ( 2005; ). Photosynthetic nitrate assimilation in cyanobacteria. Photosynth Res 83, 117–133.[CrossRef]
    [Google Scholar]
  19. Frias, J. E., Flores, E. & Herrero, A. ( 1994; ). Requirement of the regulatory protein NtcA for the expression of nitrogen assimilation and heterocyst development genes in the cyanobacterium Anabaena sp. PCC 7120. Mol Microbiol 14, 823–832.[CrossRef]
    [Google Scholar]
  20. Fujiki, H. & Suganuma, M. ( 1999; ). Unique features of the okadaic acid activity class of tumor promoters. J Cancer Res Clin Oncol 125, 150–155.[CrossRef]
    [Google Scholar]
  21. Guerrero, M. G. & Lara, C. ( 1987; ). Assimilation of inorganic nitrogen. In The Cyanobacteria, pp. 163–185. Edited by P. Fay & C. Van Baalen. Amsterdam: Elsevier Science.
  22. Herrero, A., Muro-Pastor, A. M. & Flores, E. ( 2001; ). Nitrogen control in cyanobacteria. J Bacteriol 183, 411–425.[CrossRef]
    [Google Scholar]
  23. Huang, X., Dong, Y. & Zhao, J. ( 2004; ). HetR homodimer is a DNA-binding protein required for heterocyst differentiation, and the DNA-binding activity is inhibited by PatS. Proc Natl Acad Sci U S A 101, 4848–4853.[CrossRef]
    [Google Scholar]
  24. Kahru, M., Horstmann, U. & Rud, O. ( 1994; ). Satellite detection of increased cyanobacteria blooms in the Baltic Sea: natural fluctuation or ecosystem change?. Ambio 23, 469–472.
    [Google Scholar]
  25. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.[CrossRef]
    [Google Scholar]
  26. Lehtimäki, J., Moisander, P., Sivonen, K. & Kononen, K. ( 1997; ). Growth, nitrogen fixation, and nodularin production by two Baltic Sea cyanobacteria. Appl Environ Microbiol 63, 1647–1656.
    [Google Scholar]
  27. Lundberg, C., Lonnroth, M., von Numers, M. & Bonsdorff, E. ( 2005; ). A multivariate assessment of coastal eutrophication. Examples from the Gulf of Finland, northern Baltic Sea. Mar Pollut Bull 50, 1185–1196.[CrossRef]
    [Google Scholar]
  28. Meeks, J. C. & Castenholz, R. W. ( 1971; ). Growth and photosynthesis in an extreme thermophile, Synechococcus lividus (Cyanophyta). Arch Mikrobiol 78, 25–41.[CrossRef]
    [Google Scholar]
  29. Meeks, J. C. & Elhai, J. ( 2002; ). Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol Mol Biol Rev 66, 94–121.[CrossRef]
    [Google Scholar]
  30. Meeks, J. C., Wycoff, K. L., Chapman, J. S. & Enderlin, C. S. ( 1983; ). Regulation of expression of nitrate and dinitrogen assimilation by Anabaena species. Appl Environ Microbiol 45, 1351–1359.
    [Google Scholar]
  31. Muro-Pastor, A. M., Valladares, A., Flores, E. & Herrero, A. ( 2002; ). Mutual dependence of the expression of the cell differentiation regulatory protein HetR and the global nitrogen regulator NtcA during heterocyst development. Mol Microbiol 44, 1377–1385.[CrossRef]
    [Google Scholar]
  32. Ohmori, M. & Hattori, A. ( 1972; ). Effect of nitrate on nitrogen-fixation by the blue-green alga Anabaena cylindrica. Plant Cell Physiol 13, 589–599.
    [Google Scholar]
  33. Ohta, T., Sueoka, E., Iida, N., Komori, A., Suganama, M., Nishiwaki, R., Tatematsu, M., Kim, S. J., Carmichael, W. W. & Fukiki, H. ( 1994; ). Nodularin, a potent inhibitor of protein phosphatases 1 and 2A, is a new environmental carcinogen in male F344 rat liver. Cancer Res 54, 6402–6406.
    [Google Scholar]
  34. Raateoja, M., Seppala, J., Kuosa, H. & Myrberg, K. ( 2005; ). Recent changes in trophic state of the Baltic Sea along SW coast of Finland. Ambio 34, 188–191.
    [Google Scholar]
  35. Risser, D. D. & Callahan, S. M. ( 2007; ). Mutagenesis of hetR reveals amino acids necessary for HetR function in the heterocystous cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 189, 2460–2467.[CrossRef]
    [Google Scholar]
  36. Sanz-Alférez, S. & del Campo, F. F. ( 1994; ). Relationship between nitrogen fixation and nitrate metabolism in the Nodularia strains M1 and M2. Planta 194, 339–345.[CrossRef]
    [Google Scholar]
  37. Sivonen, K., Kononen, K., Esala, A.-L. & Niemelä, S. I. ( 1989; ). Toxicity and isolation of the cyanobacterium Nodularia spumigena from the southern Baltic Sea in 1986. Hydrobiologia 185, 3–8.[CrossRef]
    [Google Scholar]
  38. Stalnacke, P., Grimvall, A., Sundblad, K. & Tonderski, A. ( 1999; ). Estimation of riverine loads of nitrogen and phosphorus to the Baltic Sea, 1970–1993. Environ Monit Assess 58, 173–200.[CrossRef]
    [Google Scholar]
  39. Stewart, W. D. P. & Rowell, P. ( 1975; ). Effects of l-methionine-dl-sulfoximine on assimilation of newly fixed NH3, acetylene reduction and heterocyst production in Anabaena cylindrica. Biochem Biophys Res Commun 65, 846–855.[CrossRef]
    [Google Scholar]
  40. Thiel, T. & Leone, M. ( 1986; ). Effect of glutamine on growth and heterocyst differentiation in the cyanobacterium Anabaena variabilis. J Bacteriol 168, 769–774.
    [Google Scholar]
  41. Van Baalen, C. ( 1987; ). Nitrogen fixation. In The Cyanobacteria, pp. 187–198. Edited by P. Fay & C. Van Baalen. Amsterdam: Elsevier Science.
  42. Vega-Palas, M. A., Flores, E. & Herrero, A. ( 1992; ). NtcA, a global nitrogen regulator from the cyanobacterium Synechococcus that belongs to the Crp family of bacterial regulators. Mol Microbiol 6, 1853–1859.[CrossRef]
    [Google Scholar]
  43. Voss, M., Larsen, B., Leivuori, M. & Vallius, H. ( 2000; ). Stable isotope signals of eutrophication in Baltic Sea sediments. J Mar Syst 25, 287–298.[CrossRef]
    [Google Scholar]
  44. Wei, T. F., Ramasubramanian, T. S. & Golden, J. W. ( 1994; ). Anabaena sp. strain PCC 7120 ntcA gene required for growth on nitrate and heterocyst development. J Bacteriol 176, 4473–4482.
    [Google Scholar]
  45. Wilson, K. ( 1998; ). Preparation of genomic DNA from bacteria. In Current Protocols in Molecular Biology, pp. 2.4.1–2.4.5. Edited by F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith & K. Struhl. New York: Wiley.
  46. Wolk, C. P. ( 1982; ). Heterocysts. In The Biology of Cyanobacteria, pp. 359–386. Edited by N. G. Carr & B. A. Whitton. Oxford: Blackwell Scientific Publications.
  47. Wolk, C. P. ( 2000; ). Heterocyst formation in Anabaena. In Prokaryotic Development, pp. 83–104. Edited by Y. V. Brun & L. J. Shimkets. Washington, DC: American Society for Microbiology.
  48. Wulff, F., Stigebrandt, A. & Rahm, L. ( 1990; ). Nutrient dynamics of the Baltic Sea. Ambio 19, 126–133.
    [Google Scholar]
  49. Yoon, H. S. & Golden, J. W. ( 1998; ). Heterocyst pattern formation controlled by a diffusible peptide. Science 282, 935–938.[CrossRef]
    [Google Scholar]
  50. Zhang, C. C., Laurent, S., Sakr, S., Peng, L. & Bedu, S. ( 2006; ). Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals. Mol Microbiol 59, 367–375.[CrossRef]
    [Google Scholar]
  51. Zhou, R., Cao, Z. & Zhao, J. ( 1998; ). Characterization of HetR protein turnover in Anabaena sp. PCC 7120. Arch Microbiol 169, 417–423.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/007849-0
Loading
/content/journal/micro/10.1099/mic.0.2007/007849-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error