Growth inhibition of cultured marine phytoplankton by toxic algal-derived polyunsaturated aldehydes

Abstract

Several marine diatoms produce polyunsaturated aldehydes (PUAs) that have been shown to be toxic to a wide variety of model organisms, from bacteria to invertebrates. However, very little information is available on their effect on phytoplankton. Here, we expand previous studies to six species of marine phytoplankton, belonging to different taxonomic groups that are well represented in marine plankton. The effect of three PUAs, 2 E,4 E-decadienal, 2 E,4 E-octadienal and 2 E,4 E-heptadienal, was assessed on growth, cell membrane permeability, flow cytometric properties and morphology. A concentration-dependent reduction in the growth rate was observed for all cultures exposed to PUAs with longer-chained aldehydes having stronger effects on growth than shorter-chained aldehydes. Clear differences were observed among the different species. The prymnesiophyte Isochrysis galbana was the most sensitive species to PUA exposure with a lower threshold for an observed effect triggered by mean concentrations of 0.10 μmol L −1 for 2 E,4 E-decadienal, 1.86 μmol L −1 for 2 E,4 E-octadienal and 3.06 μmol L −1 for 2 E,4 E-heptadienal, and a 50% growth inhibition (EC 50) with respect to the control at 0.99, 2.25 and 5.90 μmol L −1 for the three PUAs, respectively. Alternatively, the chlorophyte Tetraselmis suecica and the diatom Skeletonema marinoi (formerly S. costatum) were the most resistant species with 50% growth inhibition occurring at concentrations at least two to three times higher than I. galbana. In all species, the three PUAs caused changes in flow cytometric measures of cell size and cell granulosity and increased membrane permeability, assessed using the viability stain SYTOX Green. For example, after 48 h 51.6 ± 2.6% of I. galbana cells and 15.0 ± 1.8% of S. marinoi cells were not viable. Chromatin fragmentation was observed in the dinoflagellate Amphidinium carterae while clear DNA degradation was observed in the chlorophyte Dunaliella tertiolecta. Concentrations used are in a significant range for affecting growth and performance of phytoplankton living in close vicinity of PUA-producing algae. Thus, PUAs may act as allelochemicals by mediating interactions among planktonic organisms.