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Evaluation of the grazer–prey interaction as a biotechnological strategy to increase toxin production by dinoflagellate cultures in photobioreactors

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Abstract

In this paper, we extend an existing approach to biotechnologically assess grazer–prey interactions between the crustacean Artemia salina (grazer) and the toxic dinoflagellate Protoceratium reticulatum (prey). The applied strategy is presented as a bioprocessing tool for enhancing the production of toxins and bioactive compounds in dinoflagellate cultures. Interactions were based on direct and indirect contact between the grazer and the prey, as well as on the use of different extracts from A. salina cysts and supernatants from cultures in which A. salina had been grown. Several treatments were found to stimulate the growth and yessotoxin production of P. reticulatum mainly due to the action of dissolved excreted substances and/or metabolites released and/or extracted from A. salina. One of the best results was obtained with a culture medium formulation containing 10 % (v/v) supernatant from a culture of A. salina nauplii. This treatment was scaled up to a 15-L photobioreactor. The average maximum specific growth rate (μ max) of P. reticulatum in this photobioreactor, operated in batch mode, increased by 27 %, whereas the maximum cell concentration (C max) decreased by 20 % relative to the corresponding control culture. An average increase in yessotoxin production of 50 % with respect to the control culture was observed.

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References

  • Ajuzie CC (2007) Palatability and fatality of the dinoflagellate Prorocentrum lima to Artemia salina. J Appl Phycol 19:513–519

    Article  Google Scholar 

  • Bergkvist J, Selander E, Pavia H (2008) Induction of toxin production in dinoflagellates: the grazer makes a difference. Oecologia 156:147–154

    Article  PubMed  Google Scholar 

  • Beuzenberg V, Mountfort D, Holland P, Shi F, Mackenzie L (2012) Optimization of growth and production of toxins by three dinoflagellates in photobioreactor cultures. J Appl Phycol 24:1023–1033

    Article  CAS  Google Scholar 

  • Burkholder JM, Glibert PM, Skelton HM (2008) Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8:77–93

    Article  CAS  Google Scholar 

  • Colin SP, Dam HG (2003) Effects of the toxic dinoflagellate Alexandrium fundyense on the copepod Acartia hudsonica: a test of the mechanisms that reduce ingestion rates. Mar Ecol Prog Ser 248:55–65

    Article  Google Scholar 

  • Fistarol GO, Legrand C, Selander E, Hummert C, Stolte W, Granéli E (2004) Allelopathy in Alexandrium spp.: effect on a natural plankton community and on algal monocultures. Aquat Microb Ecol 35:45–56

    Article  Google Scholar 

  • Fuentes-Grünewald C, Garcés E, Alacid E, Rossi S, Camp J (2012) Biomass and lipid production of dinoflagellates and raphidophytes in indoor and outdoor photobioreactors. Mar Biotechnol 15:37–47

    Article  PubMed  CAS  Google Scholar 

  • Gallardo-Rodríguez J, Sánchez-Mirón A, García-Camacho F, López-Rosales L, Chisti Y, Molina-Grima E (2012a) Bioactives from microalgal dinoflagellates. Biotechnol Adv 30:1673–1684

    Article  PubMed  CAS  Google Scholar 

  • Gallardo-Rodríguez JJ, García-Camacho F, Sánchez-Mirón A, López-Rosales L, Chisti Y, Molina-Grima E (2012b) Shear-induced changes in membrane fluidity during culture of a fragile dinoflagellate microalga. Biotechnol Prog 28:467–473

    Article  PubMed  CAS  Google Scholar 

  • Gallardo-Rodríguez JJ, Sánchez-Mirón A, García-Camacho F, Cerón-García MC, Belarbi EH, Chisti Y, Molina-Grima E (2011) Carboxymethyl cellulose and Pluronic F68 protect the dinoflagellate Protoceratium reticulatum against shear-associated damage. Bioproc Biosyst Eng 34:3–12

    Article  CAS  Google Scholar 

  • García-Camacho F, Gallardo-Rodríguez JJ, Sánchez-Mirón A, Belarbi EH, Chisti Y, Molina-Grima E (2011a) Photobioreactor scale-up for a shear-sensitive dinoflagellate microalga. Process Biochem 46:936–944

    Article  CAS  Google Scholar 

  • García-Camacho F, Gallardo-Rodríguez JJ, Sánchez-Mirón A, Cerón-García MC, Belarbi EH, Molina-Grima E (2007) Determination of shear stress thresholds in toxic dinoflagellates cultured in shaken flasks. Implications in bioprocess engineering. Process Biochem 42:1506–1515

    Article  CAS  Google Scholar 

  • García-Camacho F, Gallardo-Rodríguez JJ, Sánchez-Mirón A, Chisti Y, Molina-Grima E (2011b) Genetic algorithm-based medium optimization for a toxic dinoflagellate microalga. Harmful Algae 10:697–701

    Article  Google Scholar 

  • Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum, New York, pp 26–60

    Google Scholar 

  • Guillard RRL, Hargraves PE (1993) Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32:234–236

    Article  Google Scholar 

  • Heredia-Tapia A, Arredondo-Vega BO, Nuñez-Vázquez EJ, Yasumoto T, Yasuda M, Ochoa JL (2002) Isolation of Prorocentrum lima (Syn. Exuviaella lima) and diarrhetic shellfish poisoning (DSP) risk assessment in the Gulf of California, Mexico. Toxicon 40:1121–1127

    Article  PubMed  CAS  Google Scholar 

  • John U, Tillmann U, Medlin LK (2002) A comparative approach to study inhibition of grazing and lipid composition of a toxic and non-toxic clone of Chrysochromulina polylepis (Prymnesiophyceae). Harmful Algae 1:45–57

    Article  CAS  Google Scholar 

  • Keller MD, Guillard RRL (1986) Factors significant to marine dinoflagellate culture. In: Anderson DM, White AW, Baden DG (eds) Toxic dinoflagellates. Elsevier, New York, pp 113–116

    Google Scholar 

  • Mæland A, Rønnestad I, Fyhn HJ, Berg L, Waagbø R (2000) Water-soluble vitamins in natural plankton (copepods) during two consecutive spring blooms compared to vitamins in Artemia franciscana nauplii and metanauplii. Mar Biol 136:765–772

    Article  Google Scholar 

  • Naz M (2008) The changes in the biochemical compositions and enzymatic activities of rotifer (Brachionus plicatilis Müller) and Artemia during the enrichment and starvation periods. Fish Physiol Biochem 34:391–404

    Article  PubMed  CAS  Google Scholar 

  • Ozaki Y, Kaneko G, Hakuno F, Takahashi S-I, Watabe S (2013) Insulin/insulin-like growth factor-like activity in the aqueous extracts of the rotifer Brachionus plicatilis. Fish Sci 79:47–53

    Article  CAS  Google Scholar 

  • Paz B, Riobó P, Luisa Fernández M, Fraga S, Franco JM (2004) Production and release of yessotoxins by the dinoflagellates Protoceratium reticulatum and Lingulodinium polyedrum in culture. Toxicon 44:251–258

    Article  PubMed  CAS  Google Scholar 

  • Selander E, Thor P, Toth G, Pavia H (2006) Copepods induce paralytic shellfish toxin production in marine dinoflagellates. Proc R Soc B 273:1673–1680

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Strom S, Wolfe G, Holmes J, Stecher H, Shimeneck C, Lambert S, Moreno E (2003) Chemical defense in the microplankton I: feeding and growth rates of heterotrophic protists on the DMS-producing phytoplankter Emiliania huxleyi. Limnol Oceanogr 48:217–229

    Article  CAS  Google Scholar 

  • Tan ZJ, Yan T, Yu RC, Zhou MJ (2007) Transfer of paralytic shellfish toxins via marine food chains: a simulated experiment. Biomed Environ Sci 20:235–241

    PubMed  CAS  Google Scholar 

  • Turner JT, Tester PA (1998) Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs. Limnol Oceanogr 42:1203–1214

    Article  Google Scholar 

  • Van Stappen G (1996) Artemia. In: Lavens P, Sorgeloos P (eds) Manual on the production and use of live food for aquaculture. FAO Fisheries Technical Paper. Food and Agriculture Organization of the United Nations, Rome, pp 79–250

    Google Scholar 

  • Zhengxing W, Yinglin Z, Mingyuan Z, Zongling W, Dan W (2006) Effects of toxic Alexandrium species on the survival and feeding rates of brine shrimp, Artemia salina. Acta Ecol Sin 26(12):3942-3947

    Google Scholar 

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Acknowledgments

This research was funded by the Spanish Ministry of Science and Innovation (CTQ2008-06754-C04-02/PPQ), the Spanish Ministry of Education and Science (SAF2011-28883-C03-02) and the European Regional Development Fund Program.

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Correspondence to F. García-Camacho.

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López-Rosales, L., Gallardo-Rodríguez, J.J., Sánchez-Mirón, A. et al. Evaluation of the grazer–prey interaction as a biotechnological strategy to increase toxin production by dinoflagellate cultures in photobioreactors. J Appl Phycol 26, 257–263 (2014). https://doi.org/10.1007/s10811-013-0092-6

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  • DOI: https://doi.org/10.1007/s10811-013-0092-6

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