Effect of nitrate and phosphate concentration on production of microcystins by Microcystis viridis NIES 102

Authors

  • K. Kameyama Doctoral Program in Agricultural Sciences, University of Tsukuba, Tsukuba, Japan
  • N. Sugiura Institute of Agricultural and Forest Engineering, University of Tsukuba, Tsukuba, Japan
  • H. Isoda National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba 305–8506 Japan
  • Y. Inamori National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba 305–8506 Japan
  • T. Maekawa Institute of Agricultural and Forest Engineering, University of Tsukuba, Tsukuba, Japan

Keywords:

growth phase

Abstract

The effects of nitrate and phosphate concentrations on the production of three microcystins, namely, types LR, RR and YR by Microcystis viridis NIES 102, were determined in batch culture experiments at in situ level concentrations. The yield of microcystin‐RR during the exponential growth phase increased favorably in nitrate concentrations ranging from 0.2 to 0.8 mg l−1 of NO3-N. The effect plateaued at 1.0 mg l−1. This tendency was similar to the effect of nitrate on the specific growth rate. There was no significant correlation between the amounts of intracellular microcystins at exponential growth phase and nitrate concentrations. On the other hand, the specific growth rate was constant regardless of the phosphate concentrations. However, the yield of the three types of microcystins in the culture broth and the amounts of intracellular microcystins decreased with increasing the phosphate concentration. Furthermore, it was found that the correlation between total yield of microcystins (LR, RR and YR) and the ratio of microcystins during the exponential growth phase showed almost constant values, as follows: microcystin LR (0.24), RR (0.66) and YR (0.10).

References

Arment, A. R. and Carmichael, W.W. 1996. Evidence that microcystin is a thio-template product. J. Phycol., 32: 591–597.

Benning, C., Huang, Z. H. and Gage, D. A. 1995. Accumulation of a novel glycolipid and a betaine lipid in cells of Rhodobactersphaeroides grown under phosphate limitation. Arch Biochem Biophys, 317: 103–111.

Carmichael, W.W., Tones, C. L. A., Mahmood, N. A. and Theiss, W. C. 1985. Algal toxins and water-based diseases. CPC Crit. Rev.Environ. Control., 15: 275–283.

Carmichael, W.W., Beasley, V., Bunner, D. L., Eloff, J. N., Falconer, I., Gorham, P., Harada, K., Krishnamurthy, T., Yu, M. J., Moore, R. E., Rinehart, K., Runnegar, M., Skulberg, O. M. and Watanabe, M. 1988. Naming of cyclic heptapeptide toxins of cyanobacteri a(blue-green algae). Toxicon, 26: 971–973.

Carmichael, W.W. 1992. Cyanobacteri a secondary metabolites: The cyanotoxins. J. Appl. Bacteriol., 72: 445–459.

Dittmann, E., Neilan, B. A., Erhard, M., Doren, H. V. and Borner, T. 1997. Insertional mutagenesi s of peptide synthetase gene thatis responsible for hepatotoxin production in the cyanobacterium Microcystis aeruginosa PCC7806. Mol.Microbiol., 26: 779–787.

Enterprise Bureau of Ibaraki Prefecture, Japan, 1982-1996. Annual reports ofwater quality of Enterprise Bureau, Nos. 14-28. IbarakiPrefectrure, Japan (In Japanese).

Falconer, I. R., Beresford, A. M. and Runnegar, M. T. 1983. Evidenceof liver damage by toxin from a bloom of the blue-green alga, Microcystis aeruginosa. Med. J. Aust., 28: 511–514.

Fastner, J., Erhard, M., Carmichael, W. W., Sun, F., Rinehart, K. L., Ronicke, H. and Chorus, I. 1999. Characterization and diversityof microcystins in natural blooms and strains of the genera Microcystis and Planktothrix from German freshwaters. Arch.Hydrobiol., 145: 147–163.

Harada, K.-I., Matsuura, K., Suzuki, M., Oka, H., Watanabe, M. F., Oishi, S., Dahlem, A. M., Beasley, V. R. and Carmichael, W. W. 1988. Analysis and puri. cation of toxic peptide fromcyanobacte-ria by reversed-phas e high-performanc e liquid chromatography. J. Chromatogr., 448: 275–283.

Harada, K.-I., Ogawa, K., Kimura, Y., Murata, H., Suzuki, M., Thorn, P. M., Evans, W. R. and Carmichael, W. W. 1991. Microcystinsfrom Anabaena os-aquae NRC 525-17. Chem. Res. Toxicol., 4: 535–540.

Kearns, K.D. and Hunter, M.D. 2000. Green algal extracellular products regulate antialgal toxin production in a cyanobacterium. Environ.Microbiol., 2: 291–297.

Kotak, B. G., Lam, A. K.-Y., Prepas, E. E. and Hrudey, S. E. 2000. Role of chemical and physical variables in regulating microcystin-LRconcentration in phytoplankton of eutrophic lakes. Can. J. Fish. Aquat. Sci., 57: 1584–1593.

Krishnamurthy, T., Carmichael, W. W. and Sarver, E. W. 1986. Toxic peptides fromfreshwater cyanobacteri a (blue-green algae). I. Isolationpuri. cation and characterization of peptides from Microcystis aeruginosa and Anabaena os-aquae. Toxicon, 24: 865–873.

Krishnamurthy, T., Szafraniec, L., Hunt, D. F., Shabanowitz, J., Yates, J. R., Hauer, C. R., Carmichael, W. W., Skulberg, O., Codd, G.A. and Missler, S. 1989. Structural characterization of toxic cyclic peptides from blue-green algae by tandem mass spectrometry. Proc. Natl. Acad. Sci. USA., 86: 770–774.

Lee, S. J., Jang, M.-H., Kim, H.-S., Yoon, B.-D. and Oh, H.-M. 2000. Variation of microcystin content of Microcystis aeruginosa relativeto medium N:P ratio and growth stage. J. Appl. Microbiol., 89: 323–329.

Long, B. M., Jones, G. J. and Orr, P. T. 2001. Cellular microcystin content in N-limited Microcystis aeruginosa can be predicted fromgrowth rate. Appl. Environ. Microbiol., 67: 278–283.

Oh, H.-M., Lee, S. J., Jang, M.-H. and Yoon, B.-D. 2000. Microcystinproduction by M. aeruginosa in a phosphorus-limited chemostat. Appl. Environ. Microbiol., 66: 176–179.

Orr, P. T. and Jones, G. J. 1998. Relationship between microcystinproduction and cell division rate in nitrogen limited Microcystisaeruginosa cultures. Limnol. Oceanogr., 43: 1604–1614.

Palmstrom, N. S., Carlson, R. E. and Cooke, G. D. 1988. Potential links between eutrophication and formation of carcinogens in drinkingwater. Lake Reservoir Mgmt., 4: 1–15.

Rapala, J., Sivonen, K., Lyra, C. and Niemela, S. I. 1997. Variation of microcystins, cyanobacterial hepatotoxins , in Anabaena spp. as afunction of growth stimuli. Appl. Environ. Microbiol., 63: 2206–2212.

Rinehart, K. L., Namikoshi, M. and Choi, B. W. 1994. Structure and biosynthesis of toxin toxins from blue-green algae (cyanobacte -ria). J. Appl. Phycol., 6: 159–176.

Shi, L., Carmichael, W. W. and Miller, I. 1995. Immuno-gold localization of hepatotoxins in cyanobacterial cells. Arch Microbiol., 163: 7–15.

Sivonen, K. 1990. Effect of light, temperature, nitrate, orthophosphate, and bacteria on growth of and hepatotoxin productionby Oscillatoria agarghi i strains. Appl. Environ. Microbiol., 56: 2658–2666.

Sivonen, K. 1996. Cyanobacteria l toxins and toxin production. Phycologia, 35: 12–24.

Song, L., Sano, T., Li, R., Watanabe, M.M., Liu, Y. and Kaya, K. 1998. Microcystis viridis (cyanobacteria ) under different culture conditions.Phycol. Res., 46: 19–23.

Turner, P. C., Gammie, A., Hollinrake, K. and Codd, G. A. 1990. Pneumonia associated with contact with cyanobacteria. Br. Med. J., 300: 1440–1441.

Utkilen, H. and Gjolme, N. 1992. Toxin production by Microcystis aeruginosa as a function of light in continuous cultures andits ecological signi. cance. Appl. Environ. Microbiol., 58: 1321–1325.

Utkilen, H. and Gjolme, N. 1995. Iron-stimulated toxin production in Microcystis aeruginosa. Appl. Environ.Microbiol., 61: 797–800.

Walsh, K., Jones, G. J. and Dunstan, R. H. 1997. Effect of irradiance on fatty acid, carotenoid, total protein concentration andgrowth of Microcystis aeruginosa. Phytochemistry, 44: 817–824.

Watanabe, M. F., Harada, K.-I., Matsuura, K., Watanabe, M. and Suzuki, M. 1989. Heptapeptide toxin production during the batch cultureof two Microcystis species (cyanobacteria). J. Appl. Phycol., 1: 161–165.

Wei, B., Sugiura, N. and Maekawa, T. 2001. Use of arti. cial neural network in the prediction of algal blooms. Wat. Res., 35: 2022–2028.

WHO (World Health Organization). 1998. Guidelines for drinkingwater quality , 2nd ed., Addendum to Vol. 1, 13–14. Rome: Recommendations.

Yagi, O., Inamori, Y. and Inagaki, N. 1986. Puri. cation of Microcystis aeruginosa. Res. Rep. Natl. Inst. Environ. Stud. Japan., 92: 7–17.

Published

2002-12-01

Issue

Section

Research article