Food uptake in the harmful alga Prymnesium parvum mediated by excreted toxins

Toxin production is widespread among aquatic microalgae, suggesting a functional advantage for organisms producing toxic compounds. However, the biological role of algal toxin production is only vaguely understood. Here, we show that excretion of a toxic substance in the phagotrophic phytoflagellate Prymnesium parvum (Prymnesiophyceae) constitutes a mechanism to immobilize and seize motile prey. Feeding frequency of P. parvum in dilute batch cultures was low when fed the motile prey Heterocapsa rotundata (dinoflagellate). However, dense cultures caused immobilization of H. rotundata cells, thereby allowing P. parvum to feed on them. In contrast, when fed a nonmotile prey—the diatom Thalassiosira pseudonana—feeding frequency was high, even in dilute P. parvum cultures. We could demonstrate that feeding frequency of P. parvum on H. rotundata was positively correlated with the measure of the toxic effect causing immobilization and lysis of prey cells. The fact that the toxic effect on H. rotundata was found in cell-free filtrate of P. parvum cultures suggests that immobilization and lysis of prey cells were caused by the excretion of toxins. Blooms of planktonic algae are common in aquatic environments, and harmful algal blooms cause substantial commercial problems for the exploitation of marine and freshwater resources, as well as for recreational purposes (e.g., Hallegraeff 1993). The harmful effects of algal blooms are typically from toxins produced by the algae. The question of why algae produce toxins has, therefore, been a point of much speculation, but few facts exist on possible biological or ecophysiological roles of toxin production. Toxins might function as grazing deterrents (Verity and Stoecker 1982). Another possibility is that toxin-producing algae inhibit and thereby outcompete other phytoplankton competitors through the release of allelopathic substances (Maestrini and Bonin 1981; Schmidt and Hansen 2001). It has also been suggested that some toxic substances produced by algae primarily function as hormones or regulate ion channels (Turner et al. 1998). In this report, we present data on the role of toxin excretion by a toxic alga, the prymnesiophyte flagellate Prymnesium parvum in feeding. The species is mixotrophic (i.e., it is photosynthetic), but it also feeds phagotrophically on other microorganisms, such as bacteria (Nygaard and Tobiesen 1993) and other protists (Tillmann 1998, P. parvum f. patelliferum [Green, Hibberd et Pienaar] A. Larsen). Blooms of P. parvum occur in brackish and coastal waters where they have caused much damage to the aquaculture industry (Reich and Aschner 1947; Moestrup 1994). Most P. parvum blooms have been reported from Europe, but the species is ubiquitous and has caused toxic blooms worldwide (Moes1 Present address: Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar, CMIMA-CSIC, Passeig Marı́tim 37-49, 08003 Barcelona, Spain ([email protected]).