Multiple biological responses and transcriptome plasticity of the model unicellular eukaryote Paramecium for cadmium toxicity aggravated by freshwater acidification

Cadmium (Cd) pollution is a widespread threat to aquatic life, and ongoing freshwater acidification (FA) can be expected to interact with Cd compounds to disrupt freshwater ecosystems. However, the effects of FA on Cd biotoxicity remain unclear. Herein, the model ciliate Paramecium tetraurelia, a model unicellular eukaryotic organism, was used to explore the response to environmental relevant concentrations of Cd under acidification conditions. We show for the first time that exposure to acidified freshwater accelerated Cd bioaccumulation and enhanced Cd bioavailability in P. tetraurelia, suggesting the synergistic interaction of Cd and FA. The co-exposure greatly reduced the abundance and carbon biomass, altered lysosomal membrane stability, induced oxidative stress, and consumed more ATP in exposed ciliates. Transcriptome plasticity enabled P. tetraurelia to develop a Cd stress-adaptive transcriptional profile (upregulation of transport and detoxification and downregulation of energy metabolism) under acidification. With a concomitant inhibition in energy production, the exposed ciliates might have diverted the energy from growth and cell replication to compensate for the energetic cost from stress response and detoxification. Collectively, acidified freshwater could aggravate Cd toxicity, which, in turn, arouses the response strategy of ciliates to cope with stress, providing a mechanistic understanding of the interaction between freshwater acidification and Cd pollution in the basic trophic level ciliated protozoa in freshwater ecosystems.