Maira Maselli:
Eco-physiology of prey generalist mixoplanktonic ciliates

Date: 28-05-2021    Supervisor: Per Juel Hansen




Ciliates have a pivotal role in the ecology of marine systems, as they are an important trophic link between the microbial loop and metazoan grazers. Many planktonic ciliates retain functional chloroplasts from the photosynthetic prey that they ingest. This enable them to photosynthesize and thereby being mixotrophs. While some species express a selective behavior towards specific prey types from which they acquire chloroplasts, the majority of species among the oligotrich ciliates can acquire chloroplasts from different algal prey types and are defined as prey generalist. The focus on this thesis was on ecology and the physiology of these organisms based on laboratory experiments on cultures of Strombidium spp. In addition to this, a field survey was carried out on four Greenlandic fjords that receives high amounts of glacier flour to assess the role of mixotrophs in these systems.

Cultures of three Strombidium species were established from single cells isolated from their natural environment and identified via sequencing of their ribosomal subunits genes. The growth of the three Strombidium species in culture was best sustained when they were fed cryptophytes and chlorophytes as prey. However other algal prey types within the size range of 2 and 12 µm could also sustain their growth. Based on these observations, the cryptophyte Teleaulax amphioxeia was selected as prey in the subsequent experiments.

The relative contributions of photosynthesis to the total carbon uptake was estimated for S. cf. basimorphum and S. cf. conicum, when acclimated to different prey abundances. Inorganic carbon incorporation via photosynthesis was only quantitatively relevant when prey availability was low and it led to increased gross growth efficiencies in this condition if compared with purely heterotrophic ciliates species. Strombidium cf. basimorphum and S. cf. conicum displayed differences in the ability to maintain the sequestered chloroplasts during prey starvation. Strombidium cf. basimorphum seemed to exploit efficiently the chloroplasts when starved of prey, while that was not the case for S. cf. conicum.

The use of molecular markers demonstrated that genetic material from prey nuclei, nucleomorphs and ribosomes were detectable in S. cf. basimorphum for at least five days after prey ingestion. Transcripts of prey nuclear origin were also found in starved cells of S. cf. basimorphum. The functionality of sequestered chloroplasts in S. cf. basimorphum was affected during prey starvation, when exposed to relatively higher irradiances. However, at higher irradiance levels, the ciliates had higher photosynthetic rates when supplied with prey abundances that saturated its growth.

The availability of dissolved inorganic nitrogen and phosphorus in the media had no effects on the starvation responses in Strombidium cf. basimorphum, as the ciliates seem unable to take up and utilize these inorganic nutrients for growth. Nutrient concentration, however, affected the physiology and the stoichiometry of the prey; thus indirectly affecting the ciliate, which maximized its growth and ingestion rates when grown under nutrient depleted conditions.

The total biomass of mixotrophic ciliates in Greenlandic fjords and their relative abundance compared to the total ciliate biomass was comparable to what has been found in the same season in more open waters in the same area. Indeed, water turbidity and de-eutrophication due to glacier inputs in the fjords are not likely to affect mixotrophic ciliates abundance directly, as they rely on prey ingestion 4 to proliferate.

In addition, experiments on mixotrophic ciliates in culture demonstrated that inert sediment particles were not ingested at all, thus the sediment carried with the water runoff from glaciers does not seem to have any effects on their growth and chloroplasts turnover.