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.KEY WORDS: Uro ne ma marinum · Toxin · Phytoplankton · Bacteria · Growth rate · Physiology · Flow cytometry · FDA · Epifluorescence microscopy Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 475: [35][36][37][38][39][40][41][42][43][44][45][46][47][48] 2013 even grow (albeit slowly) in water with a salinity <10 g kg −1 (Hamilton & Preslan 1969). Uronema spp. can be found residing in sediments and are abundant in coastal waters (Anderson et al. 2009). They are free-living ciliates and can be fast swimmers (Pan et al. 2010). Variations in U. marinum growth under similar culture conditions can be ex plained as genetic variability within species as a result of habitat or geographical isolation (Pérez-Uz 1995). The highest growth rates of U. marinum (0.25 ± 0.03 h −1 ) were found in isolates from an estuarine environment (Pérez-Uz 1995).Uro ne ma marinum is mainly bacterivorous and can easily be cultured on bacteria. Bacterial genera known to be utilized by U. marinum are Chromobacterium, Ser ra tia, Vibrio, Pseudomonas and Micrococcus (Plunket & Hidu 1978). U. marinum can feed on small phytoplankton as well (Rubin & Lee 1976). Strom & Morello (1998) cultured U. marinum on relatively small phytoplankton...

Chemical ecology of marine plankton

“…111 In support of the hypothesis, increased levels of DOM were shown to spur bacterial growth initially, and later declined, aer three days, due to predation by U. marinum. 111 Another class of planktonic molecules inuencing phytoplankton cell lysis is PUAs (e.g., 45-47). 112 PUAs are hypothesized to induce synchronized cell lysis when nutrients become limited resulting in bloom collapse.…”

“…The bacterivorous ciliate, Uronema marinum, was found to release unidentied toxins that inhibited the growth of a coccolithophore, Emiliania huxleyi. 111 These toxins are also hypothesized to lyse the coccolithophore and increase the concentration of DOM available to the heterotrophic bacterial prey of U. marinum. 111 In support of the hypothesis, increased levels of DOM were shown to spur bacterial growth initially, and later declined, aer three days, due to predation by U. marinum.…”

“…111 These toxins are also hypothesized to lyse the coccolithophore and increase the concentration of DOM available to the heterotrophic bacterial prey of U. marinum. 111 In support of the hypothesis, increased levels of DOM were shown to spur bacterial growth initially, and later declined, aer three days, due to predation by U. marinum. 111 Another class of planktonic molecules inuencing phytoplankton cell lysis is PUAs (e.g., 45-47).…”