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Linking protistan community shifts along salinity gradients with cellular haloadaptation strategies
(2019)
Salinity is one of the most structuring environmental factors for microeukaryotic communities. Using eDNA barcoding, I detected significant shifts in microeukaryotic community compositions occurring at distinct salinities between brackish and marine conditions in the Baltic Sea. I, furthermore, conducted a metadata analysis including my and other marine and hypersaline community sequence data to confirm the existence of salinity-related transition boundaries and significant changes in alpha diversity patterns along a brackish to hypersaline gradient. One hypothesis for the formation of salinity-dependent transition boundaries between brackish to hypersaline conditions is the use of different cellular haloadaptation strategies. To test this hypothesis, I conducted metatranscriptome analyses of microeukaryotic communities along a pronounced salinity gradient (40 – 380 ‰). Clustering of functional transcripts revealed differences in metabolic properties and metabolic capacities between microeukaryotic communities at specific salinities, corresponding to the transition boundaries already observed in the taxonomic eDNA barcoding approach. In specific, microeukaryotic communities thriving at mid-hypersaline conditions (≤ 150 ‰) seem to predominantly apply the ‘low-salt – organic-solutes-in’ strategy by accumulating compatible solutes to counteract osmotic stress. Indications were found for both the intracellular synthesis of compatible solutes as well as for cellular transport systems. In contrast, communities of extreme-hypersaline habitats (≥ 200 ‰) may preferentially use the ‘high-salt-in’ strategy, i. e. the intracellular accumulation of inorganic ions in high concentrations, which is implied by the increased expression of Mg2+, K+, Cl- transporters and channels.
In order to characterize the ‘low-salt – organic-solutes-in’ strategy applied by protists in more detail, I conducted a time-resolved transcriptome analysis of the heterotrophic ciliate Schmidingerothrix salinarum serving as model organism. S. salinarum was thus subjected to a salt-up shock to investigate the intracellular response to osmotic stress by shifts of gene expression. After increasing the external salinity, an increased expression of two-component signal transduction systems and MAPK cascades was observed. In an early reaction, the expression of transport mechanisms for K+, Cl- and Ca2+ increased, which may enhance the capacity of K+, Cl- and Ca2+ in the cytoplasm to compensate possibly harmful Na+ influx. Expression of enzymes for the synthesis of possible compatible solutes, starting with glycine betaine, followed by ectoine and later proline, could imply that the inorganic ions K+, Cl- and Ca2+ are gradually replaced by the synthesized compatible solutes. Additionally, expressed transporters for choline (precursor of glycine betaine) and proline could indicate an intracellular accumulation of compatible solutes to balance the external salinity. During this accumulation, the up-regulated ion export mechanisms may increase the capacity for Na+ expulsion from the cytoplasm and ion compartmentalization between cell organelles seem to happen.
The results of my PhD project revealed first evidence at molecular level for the salinity-dependent use of different haloadaptation strategies in microeukaryotes and significantly extend existing knowledge about haloadaptation processes in ciliates. The results provide ground for future research, such as (comparative) transcriptome analysis of ciliates thriving in extreme-hypersaline habitats or experiments like qRT-PCR to validate transcriptome results.