A strain of the toxic dinoflagellate Karlodinium veneficum isolated from the East China Sea is an omnivorous phagotroph

Abstract

Karlodinium veneficum is a cosmopolitan, toxic, and harmful algal bloom-forming dinoflagellate, of which the mixotrophy has been suggested to be a key factor in the formation and maintaining of HABs and thus deserves more intensive explorations. Here, we report an investigation on the phagotrophy of K. veneficum using a clonal culture isolated from the coastal water of East China Sea. We found K. veneficum is an omnivorous phagotroph feeding on both live and dead bodies/cells of a fish (Oryzias melastigma), brine shrimp (Artemia salina), rotifer (Brachionus plicatilis), co-cultivated microalgae Akashiwo sanguinea, Margalefidinium polykrikoides, Alexandrium leei, Rhodomonas salina, Isochrysis galbana, and its own species. Karlodinium veneficum extracted the cell contents of all species provided through either a peduncle (i.e. myzocytosis) or by engulfing the whole cell of small preys (i.e. phagotrophy sensu stricto). Karlodinium veneficum preferred to ingest non-motile or newly dead preys, no matter whether they were fish, zooplankton, or phytoplankton. Importantly, K. veneficum exhibited micropredation on animals with sizes much larger than itself (fish, rotifer, and brine shrimp), especially when they were injured or newly dead. The LysoSensor- and LysoTracker-stained lysosomes or/and phagolysosomes of K. veneficum increased when preys were added. Cannibalism in K. veneficum, i.e. a cell feeds on other unhealthy or dead cells of the same species, was observed as the first time in the study, which can help the growth and elongated maintaining of the population under nutrient deficiency (i.e. the culture maintained viable in culture plates without nutrient supplement up to a year). The growth rate of K. veneficum exhibited significant positive correlation with ingestion rate, which differed among prey species, and the highest growth rate was observed when feeding on R. salina. The ingest ability of K. veneficum was triggered by nutrient deficiency. In conclusion, the omnivorous mixotrophy is proposed to be a key autecological mechanism for K. veneficum to widen its ecological niche and succeed in forming a cosmopolitan distribution and frequent blooms.