Skip to main content
Log in

Effects of hydrogen peroxide on the content of major volatile halogenated compounds in the red alga Asparagopsis taxiformis (Bonnemaisoniaceae)

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

The genus Asparagopsis is a prolific source of halogenated metabolites. Due to its commercial applications, it has been intensively cultivated in southern Portugal. In the present study, we assess if the internal levels of the major halogenated metabolites (bromoform and dibromoacetic acid) in Asparagopsis taxiformis can be increased with hydrogen peroxide (H2O2) addition. Previous studies with red algae showed that the production/release of bromoform can be enhanced by exogenously supplying H2O2. However, no study has assessed if H2O2 supply enhances the content of secondary metabolites within the biomass. This detail is important as the objective of the proposed research is to enhance the content of these valuable metabolites in the produced biomass. Both the activity of the haloperoxidase enzyme and the metabolite content were assessed on short-term and long-term incubation periods to H2O2. To determine the susceptibility of A. taxiformis photosynthetic performance to the imposed oxidative stress, the in vivo fluorescence of photosystem II was monitored. A. taxiformis was shown to be physiologically vulnerable to H2O2, given the observed decrease of the maximum quantum yield of photosynthesis (F v/F m). Contrary to what was expected, the presence of H2O2 inhibited the activity of the iodoperoxidase enzyme. Nevertheless, the extracted halogenated metabolites were higher over the first hours of exposure to H2O2, decreasing after 48 h. These results are probably related to the prosthetic group of the halogenated enzyme in A. taxiformis and the long-term oxidative stress damage of H2O2 exposure. Considering the objective of the proposed research, addition of H2O2 to the cultures, prior (3 h) to biomass harvesting, increases the metabolite content.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aguilera J, Dummermuth AL, Schriek R, Wiencke C (2002) Enzymatic defences against photooxidative stress induced by ultraviolet radiation in Arctic marine macroalgae. Polar Biol 25:432–441

    Google Scholar 

  • Algues et Mer SARL (2002) Method of obtaining an antibacterial and/or antifungal extract from the algae, Bonnemaisoniaceae. Inventor: J-Y. Moigne. US Patent 6,346,252B1

  • Bansemir A, Blume M, Schröder S, Lindequist U (2006) Screening of cultivated seaweeds for antibacterial activity against fish pathogenic bacteria. Aquaculture 252:79–84

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Butler A (1998) Vanadium haloperoxidases. Curr Opin Chem Biol 2:279–285

    Article  PubMed  CAS  Google Scholar 

  • Butler A, Carter-Franklin J (2004) The role of vanadium bromoperoxidase in the biosynthesis of halogenated marine natural products. Nat Prod Rep 21:180–188

    Article  PubMed  CAS  Google Scholar 

  • Butler A, Walker J (1993) Marine haloperoxidases. Chem Rev 93:1937–1944

    Article  CAS  Google Scholar 

  • Collén J, Pedersen M (1996) Production, scavenging and toxicity of hydrogen peroxide in the green seaweed Ulva rigida. Eur J Phycol 31:265–271

    Article  Google Scholar 

  • Collén J, Ekdahl A, Abrahamsson K, Pedersén M (1994) The involvement of hydrogen peroxide in the production of volatile halogenated compounds by Meristiella gelidium. Phytochemistry 36:1197–1202

    Article  Google Scholar 

  • Dummermuth AL, Karsten U, Fisch FM, König GM, Wiencke C (2003) Responses of marine macroalgae to hydrogen-peroxide stress. J Exp Mar Biol Ecol 289:103–121

    Article  CAS  Google Scholar 

  • Fenical W (1975) Halogenation in the Rhodophyta: a review. J Phycol 11:245–259

    CAS  Google Scholar 

  • Genovese G, Tedone L, Hamann MT, Morabito M (2009) The Mediterranean red alga Asparagopsis: a source of compounds against Leishmania. Mar Drugs 7:361–366

    Article  PubMed  CAS  Google Scholar 

  • Guillard RR, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve). Gran. Can J Microbiol 8:229–239

    Article  PubMed  CAS  Google Scholar 

  • Hanelt D (1996) Photoinhibition of photosynthesis in marine macroalgae. Sci Mar 60:243–248

    CAS  Google Scholar 

  • Itoh N, Izumi Y, Yamada H (1986) Characterization of non-heme type bromoperoxidase in Corallina pilulifera. J Biol Chem 261:5149–5200

    Google Scholar 

  • Marshall RA, Hamilton JT, Dring MJ, Harper DB (2003) Do vesicle cells of the red alga Asparagopsis (Falkenbergia stage) play a role in bromocarbon production? Chemosphere 52:471–475

    Article  PubMed  CAS  Google Scholar 

  • Mata L, Silva J, Schuenhoff A, Santos R (2006) The effects of light and temperature on the photosynthesis of the Asparagopsis armata tetrasporophyte (Falkenbergia rufolanosa), cultivated in tanks. Aquaculture 252:12–19

    Article  CAS  Google Scholar 

  • Mata L, Silva J, Schuenhoff A, Santos R (2007) Is the tetrasporophyte of Asparagospis armata (Bonnmeiasoniales) limited by inorganic carbon in integrated aquaculture? J Phycol 43:1252–1258

    Article  CAS  Google Scholar 

  • Mata L, Schuenhoff A, Santos R (2010) A direct comparison of the performance of the seaweed biofilters, Asparagopsis armata and Ulva rigida. J Appl Phycol. doi:10.1007/s10811-010-9504-z

  • McConnell O, Fenical W (1977) Halogen chemistry of the red alga Asparagopsis. Phytochemistry 16:367–374

    Article  CAS  Google Scholar 

  • McElvany KD, Knight LC, Welch MJ, Siuda JF, Theiler RF, Hager LP (1979) Use of bromoperoxidase, an algae enzyme, in the preparation of radiobrominated proteins. In: Hoppe HA (ed) Marine algae in pharmaceutical science. De Gruyter, Berlin, pp 429–449

    Google Scholar 

  • Moore RM, Webb M, Tokarczyk R (1996) Bromoperoxidase and iodoperoxidase enzymes and production of halogenated methanes in marine diatom cultures. J Geophys Res 101:20899–20908

    Article  CAS  Google Scholar 

  • Murphy C, Moore R, White R (2000) Peroxidases from marine microalgae. J Appl Phycol 12:507–513

    Article  CAS  Google Scholar 

  • Neidleman SL, Geigert J (1986) Biohalogenation: principles, basic roles and applications. Ellis Horwood, Chichester, p 204

    Google Scholar 

  • Ohsawa N, Ogata Y, Okada N, Itoh N (2001) Physiological function of bromoperoxidase in the marine red alga, Corallina pilulifera: production of bromoform as an allelochemical and the simultaneous elimination of hydrogen peroxide. Phytochemistry 58:683–692

    Article  PubMed  CAS  Google Scholar 

  • Paul NA, de Nys R, Steinberg PD (2006) Chemical defence against bacteria in the red alga Asparagopsis armata: linking structure with function. Mar Ecol Prog Ser 306:87–101

    Article  CAS  Google Scholar 

  • Pedersén M, Collen J, Abrahamsson K, Ekdahl A (1996) Production of halocarbons from seaweeds: an oxidative stress reaction? Sci Mar 60:257–263

    Google Scholar 

  • Salvador N, Garreta A, Lavelli L, Ribera M (2007) Antimicrobial activity of Iberian macroalgae. Sci Mar 71:101–113

    Article  Google Scholar 

  • Schuenhoff A, Mata L, Santos R (2006) The tetrasporophyte of Asparagopsis armata as a novel seaweed biofilter. Aquaculture 252:3–11

    Article  Google Scholar 

  • Sundström J, Collén J, Ekdahl A, Abrahamsson K, Pedersén M (1996) Halocarbon production and in vivo brominating activity of Euchema denticulatum. Phytochemistry 42:1527–1530

    Article  Google Scholar 

  • Verdel EF, Kline PC, Wani S, Woods AE (2000) Purification and characterization of haloperoxidases from fresh water algae Cladophora glomerata. Comp Biochem Physiol 125:179–187

    Article  CAS  Google Scholar 

  • Vilter H, Glombitza KW, Grawe A (1983) Peroxidases from Phaeophyceae. I. Extraction and detection of the peroxidases. Bot Mar 26:331–340

    Article  CAS  Google Scholar 

  • Wever R, Krenn BE (1990) Vanadium haloperoxidases. In: Chasteen ND (ed) Vanadium in biological systems: physiology and biochemistry. Kluwer, Dordrecht, pp 81–97

    Google Scholar 

  • Wever R, Tromp M, Krenn B, Marjani A, Tol M (1991) Brominating activity of the seaweed Ascophyllum nodosum: impact on the biosphere. Environ Sci Technol 25:446–449

    Article  CAS  Google Scholar 

  • Wolk CP (1968) Role of bromine in the formation of the refractile inclusions of the vesicle cells of the Bonnemaisoniaceae (Rhodophyta). Planta 78:371–378

    Article  CAS  Google Scholar 

  • Woolard FX, Moore RE, Roller PP (1979) Halogenated acetic and acrylic acids from the red alga Asparagopsis taxiformis. Phytochemistry 18:617–620

    Article  CAS  Google Scholar 

  • Zuurbier KW, Bakkenist AR, Wever R, Muijsers AO (1990) The chlorinating activity of human myeloperoxidase, high initial activity at neutral pH value and activation by electron donors. Biochim Biophys Acta 1037:140–146

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was financed by the project POCI/MAR/59659/2004 from the Fundação para a Ciência e Tecnologia, Portugal. Leonardo Mata was further financed by the Portuguese FCT PhD-scholarships (SFRH/BD/12647/2003). We would like to express our deepest gratitude to Inês Paixão and Pedro Figueiredo for their technical support, to Nicholas Paul and the anonymous reviewer’s suggestions to improve the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Leonardo Mata.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mata, L., Gaspar, H., Justino, F. et al. Effects of hydrogen peroxide on the content of major volatile halogenated compounds in the red alga Asparagopsis taxiformis (Bonnemaisoniaceae). J Appl Phycol 23, 827–832 (2011). https://doi.org/10.1007/s10811-010-9582-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-010-9582-y

Keywords

Navigation