Skip to main content
SpringerLink
Log in

Superoxide production by marine microalgae

I. Survey of 37 species from 6 classes

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

A survey was conducted for production of the reactive oxygen species superoxide by 37 species (65 strains) of microalgae including dinoflagellates, raphidophytes, chlorophytes, prasinophytes, eustigmatophytes and prymnesiophytes. Ichthyotoxic raphidophyte species of Chattonella were found to produce the highest environmental levels of superoxide (177×104 total chemiluminescence units). However, ichthyotoxic dinoflagellates (Karenia, Alexandrium) and the prymnesiophyte Prymnesium were also found to produce significant levels of superoxide (4×104, 3×104 and 5×104 chemiluminescence units, respectively), equivalent to that of other raphidophyte species of Heterosigma and Fibrocapsa (6×104 and 2×104, respectively). A direct relationship between cell size and superoxide production was observed (r2=0.94), with larger cells producing more superoxide per cell. Chattonella produced the most superoxide per cell (expressed as cellular chemiluminescence units), followed by the dinoflagellate species Karenia, Alexandrium, Takayama and Gymnodinium. Small cells, such as the raphidophyte Heterosigma and the prymnesiophyte Prymnesium produced very little superoxide per cell (cellular chemiluminescence units), but potentially could still produce high total levels of superoxide if present at high biomass levels. Species commonly used as aquaculture bivalve feeds such as Dunaliella, Tetraselmis, Nannochloropsis and Pavlova produced negligible levels of superoxide, even at high biomass. We speculate that superoxide, while not the sole ichthyotoxic principle, may play a wider role in algal toxicity than previously considered, and propose a broad classification of microalgae based upon superoxide production.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Blackburn SI, Hallegraeff GM, Bolch CJ (1989) Vegetative reproduction and sexual life cycle of the toxic dinoflagellate Gymnodinium catenatum from Tasmania, Australia. J Phycol 25:577–590

    Google Scholar 

  • Chang FH, Anderson C, Boustead NC (1990) First record of a Heterosigma (Raphidophyceae) bloom with associated mortality of cage-reared salmon in Big Glory Bay, New Zealand. N Z J Mar Freshwater 24:461–469

    Google Scholar 

  • Clark A, Nowak BF (1999) Field investigations of amoebic gill disease in Atlantic salmon, Salmo salar L., in Tasmania. J Fish Dis 22:433–443

    Google Scholar 

  • Halim Y, Labib W (1996) First recorded toxic Alexandrium minutum Halim bloom. Harmful Algal News: IOC UNESCO, no. 14

    Google Scholar 

  • Hallegraeff GM, Stanley SO, Bolch CJ, Blackburn SI (1989) Gymnodinium catenatum blooms and shellfish toxicity in southern Tasmania, Australia. In: Okaichi T, Anderson D, Nemeto T (eds) Red tides: biology, environmental science and toxicology. Elsevier, pp 77–80

  • Hillebrand H, Durselen CD, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424

    Article  Google Scholar 

  • Kim CS, Lee SG, Lee CK, Kim HG, Jung J (1999a) Reactive oxygen species as causative agents in the ichthyotoxicity of the red tide dinoflagellate Cochlodinium polykrikoides. J Plankton Res 21:2105–2115

    Google Scholar 

  • Kim D, Nakamura A, Okamoto T, Komatsu N, Oda T, Ishimatsu A, Muramatsu T (1999b) Toxic potential of the raphidophyte Olisthodiscus luteus: mediation by reactive oxygen species. J Plankton Res 21:1017–1027

    Google Scholar 

  • Kim D, Nakamura A, Okamoto T, Komatsu N, Oda T, Iida T, Ishimatsu A, Muramatsu M (2000) Mechanism of superoxide anion generation in the toxic red tide phytoplankton Chattonella marina: possible involvement of NADPH oxidase. Biochim Biophys Acta 1524:220–227

    Google Scholar 

  • Kim D, Okamoto T, Oda T, Tachibana K, Lee KS, Ishimatsu A, Matsuyama Y, Honjo T, Muramatsu M (2001) Possible involvement of the glycocalyx in the ichthyotoxicity of Chattonella marina (Raphidophyceae): immunological approach using antiserum against cell surface structures of the flagellate. Mar Biol 139:625–632

    Google Scholar 

  • Lindholm T, Öhman P, Kurki-Helasmo K, Kincaid K, Meriluoto J (1999) Toxic algae and fish mortality in a brackish-water lake in Åland, SW Finland. Hydrobiologia 397:109–120

    Google Scholar 

  • Lush GJ, Negri A, Hallegraeff GM (2001) Exotoxins produced by the toxic dinoflagellate Alexandrium minutum characterisation by radioreceptor and neuroblastoma assays during the growth cycle. In: Hallegraeff GM, Blackburn SI, Bolch CJS, Lewis R (eds) Harmful algal blooms 2000. IOC UNESCO, pp 268–271

  • Marshall JA, Munday B, Yoshizawa Y, Hallegraeff GM (2001) Effect of irradiance on superoxide production by Chattonella marina (Raphidophyceae) from South Australia and Japan. In: Hallegraeff GM, Blackburn SI, Bolch CJS, Lewis R (eds) Harmful algal blooms 2000. IOC UNESCO, pp 316–319

  • Marshall JA, Hovenden M, Oda T, Hallegraeff GM (2002) Photosynthesis does influence reactive oxygen species production in the red tide alga Chattonella marina (Raphidophyceae). J Plankton Res 142:1231–1236

    Google Scholar 

  • Marshall JA, Nichols PD, Hamilton B, Lewis RJ, Hallegraeff GM (2003) Ichthyotoxicity of Chattonella marina (Raphidophyceae) to damselfish (Acanthochromis polycanthus): the role of reactive oxygen species and free fatty acids. Harmful Algae 2:273–281

    Google Scholar 

  • Marshall JA, Ross T, Pyecroft SB, Hallegraeff GM (2004) Superoxide production by marine microalgae. II. Consequences and possible ecological role. Mar Biol (in press)

  • Oda T, Moritomi J, Kawano I, Hamaguchi S, Ishimatsu A, Muramatsu T (1995) Catalase- and superoxide dismutase-induced morphological changes and growth inhibition in the red tide phytoplankton Chattonella marina. Biosci Biotech Biochem 59:2044–2048

    Google Scholar 

  • Oda T, Nakamura A, Midori S, Kawano I, Ishimatsu A, Muramatsu T (1997) Generation of reactive oxygen species by Raphidophycean phytoplankton. Biosci Biotech Biochem 61:1658–1662

    Google Scholar 

  • Oda T, Nakamura A, Okamoto T, Ishimatsu A, Muramatsu T (1998) Lectin-induced enhancement of superoxide anion production by red tide phytoplankton. Mar Biol 131:383–390

    Google Scholar 

  • Okaichi T (1997) Red tides in the Seto Inland Sea In: Okaichi T, Yanagi T (eds) ‘Sustainable development in the Seto Inland Sea, Japan’. Terra Scientific, Tokyo, pp 251–304

    Google Scholar 

  • Okaichi T, Ochi T, Nishio S, Takano H, Matsuno K, Morimoto T, Murakami T, Shimada M (1989) The cause of fish kills associated with red tides of Chattonella antiqua (Hada) Ono. Curr Topics Mar Biotechnol 58:185–188

    Google Scholar 

  • Palenick B, Zafiriou OC, Morel FMM (1987) Hydrogen peroxide production by a marine phytoplankter. Limnol Oceanogr 32:1365–1369

    Google Scholar 

  • Rhodes LL, Haywood AJ, Ballantine WJ, MacKenzie AL (1993) Algal blooms and climate anomalies in north-east New Zealand, August-December 1992. NZ J Mar Freshwater Res 27:419–430

    Google Scholar 

  • Shimada M, Kawamoto Y, Nakatsuka Y, Watanabe M (1993) Localisation of superoxide anion in the red tide alga Chattonella antiqua. J Histochem Cytochem 41:507–511

    Google Scholar 

  • Steidinger KA, Vargo GA, Tester PA, Tomas CR (1998) Bloom dynamics and physiology of Gymnodinium breve with emphasis on the Gulf of Mexico. In: Anderson DM, Cembella AD, Hallegraeff GM (eds) Physiological ecology of harmful algal blooms. Springer, Berlin Heidelberg New York, pp 133–153

  • Tiffany MA, Barlow SB, Matey VE, Hulbert SH (2001) Chattonella marina (Raphidophyceae), a potentially toxic algae in the Salton Sea, California. Hydrobiologia 466:187–194

    Google Scholar 

  • Toyoshima T, Ozaki HS, Shimada M, Okaichi T, Murakami TH (1985) Ultrastructural alterations on chloride cells of the yellowtail Seriola quinqueradiata, following exposure to the red tide species Chattonella antiqua. Mar Biol 38:101–108

    Google Scholar 

  • Yang CZ, Albright LJ, Yousif AN (1995) Oxygen-radical-mediated effects of the toxic phytoplankter Heterosigma carterae on juvenile rainbow trout Oncorhynchus mykiss. Dis Aquat Org 23:101–108

    Google Scholar 

  • Zika RG (1984) Short-lived oxidants in natural waters. Proc Conf Gas-Liquid Chemistry of Natural Waters. Extended abstract. In: Newman L (ed) Gas-liquid chemistry of natural waters. PaperBrookhaven Natl Lab. NTIS Publ BNL, 51757, p 52

Download references

Acknowledgements

We thank the following people from the University of Tasmania: Drs. Luis Apiolaza and Mark Hovenden for mathematical enlightenment, Helen Bond of the School of Plant Science for culturing assistance, and Dr. Tom Ross for reviewing the manuscript. The work was partially supported by an Australian Research Council grant.

Author information

Author notes

  1. Judith-Anne Marshall

    Present address: Phycotec Aquaculture Environmental Management, 73 Clifton Beach Road, Clifton Beach, 7020, Tasmania, Australia

Authors and Affiliations

  1. School of Plant Science, University of Tasmania, Private Bag 55, 7001, Hobart, Tasmania, Australia

    Judith-Anne Marshall, Miguel de Salas & Gustaaf Hallegraeff

  2. Division of Biochemistry, Faculty of Fisheries, Nagasaki University, Bunkyo, 852-8521, Nagasaki, Japan

    Tatsuya Oda

Authors
  1. Judith-Anne Marshall
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Miguel de Salas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tatsuya Oda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gustaaf Hallegraeff
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Judith-Anne Marshall.

Additional information

Communicated by M.S. Johnson, Crawley

Rights and permissions

Reprints and permissions

About this article

Cite this article

Marshall, JA., de Salas, M., Oda, T. et al. Superoxide production by marine microalgae. Marine Biology 147, 533–540 (2005). https://doi.org/10.1007/s00227-005-1596-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-005-1596-7

Keywords

Search

Navigation