Phytoplankton growth inhibited by the toxic and bacterivorous ciliate Uronema marinum (Protozoa, Ciliophora)

Abstract

The ubiquitous marine ciliate Uronema marinum is mainly bacterivorous. It was therefore surprising that in a ciliate-contaminated experiment the growth rate of the phytoplankton species Emiliania huxleyi was significantly reduced. As U. marinum does not ingest E. huxleyi cells, their growth inhibition was probably caused by a toxin secreted by the ciliate, presumably a novel type of chemical interaction between ciliates and phytoplankton. A possible function of toxin secretion is to lyse algal cells that are too large for U. marinum to ingest, to increase dissolved organic matter (DOM) concentrations and hence the growth of heterotrophic bacteria, the main food source of U. marinum. To test this hypothesis U. marinum or the filtrate of U. marinum cultures was added to cultures of phytoplankton with different cell sizes. The presence of U. marinum or the filtrate of U. marinum cultures showed an inhibiting growth effect and a negative effect on the physiology of all species tested although both effects were variable between species. Diatoms appeared less sensitive than non-diatom species. U. marinum acclimatization to phytoplankton led to stronger inhibiting effects, presumably from increased toxin production. Bacterial DGGE analysis of U. marinum cultures did not reveal known toxic bacteria that might account for the observed negative effects on the phytoplankton. Bacterial growth rates in an E. huxleyi culture increased when U. marinum filtrate had been added. In mixed cultures of bacteria, E. huxleyi and U. marinum, bacterial abundance first increased, then decreased due to ciliate predation. These findings support the hypothesis that toxin secretion by U. marinum increases non-prey phytoplankton-derived DOM and stimulates the growth of the bacterial prey.