Abstract
Bacterivory is an important ecological function of protists in natural ecosystems. However, there are diverse bacterial species resistant to protistan digestion, which reduces the carbon flow to higher trophic levels. So far, a molecular biological view of metabolic processes in heterotrophic protists during predation of bacterial preys of different digestibility is still lacking. In this study, we investigated the growth performance a ciliated protozoan Tetrahymena thermophila cultivated in a bacteria-free Super Proteose Peptone (SPP) medium (control), and in the media mixed with either a digestion-resistant bacterial species (DRB) or a digestible strain of E. coli (ECO). We found the protist population grew fastest in the SPP and slowest in the DRB treatment. Fluorescence in situ hybridization confirmed that there were indeed non-digested, viable bacteria in the ciliate cells fed with DRB, but none in other treatments. Comparative analysis of RNA-seq data showed that, relative to the control, 637 and 511 genes in T. thermophila were significantly and differentially expressed in the DRB and ECO treatments, respectively. The protistan expression of lysosomal proteases (especially papain-like cysteine proteinases), GH18 chitinases, and an isocitrate lyase were upregulated in both bacterial treatments. The genes encoding protease, glycosidase and involving glycolysis, TCA and glyoxylate cycles of carbon metabolic processes were higher expressed in the DRB treatment when compared with the ECO. Nevertheless, the genes for glutathione metabolism were more upregulated in the control than those in both bacterial treatments, regardless of the digestibility of the bacteria. The results of this study indicate that not only bacterial food but also digestibility of bacterial taxa modulate multiple metabolic processes in heterotrophic protists, which contribute to a better understanding of protistan bacterivory and bacteria-protists interactions on a molecular basis.
Highlights
Heterotrophic protists are major consumers of bacteria, controlling the abundance and community composition of bacteria and regenerating nutrients for autotrophs in aquatic and soil ecosystems [1,2]
Growth Performance of T. thermophila Feeding on Digestion-Resistant Bacteria
Using comparative transcriptomics we revealed for the first time the metabolic and molecular responses that may underlie the phenotypic variations of the model protist T. thermophila under three feeding conditions, i.e., the bacteria-free medium (SPP), the medium with digestible bacteria (ECO), and the medium with digestion-resistant bacteria (BAC)
Summary
Heterotrophic protists (protozoa) are major consumers of bacteria, controlling the abundance and community composition of bacteria and regenerating nutrients for autotrophs in aquatic and soil ecosystems [1,2]. Effective ingestion and digestion of bacterial preys by protists are essential to fulfill their pivotal role in channeling organic matter and energy to higher trophic levels via the microbial loop. During this process, many bacterial species seem to have evolved a range of physiological, behavior, and chemical mechanisms to avoid being ingested (e.g., small or large cell sizes, rapid swimming, surface masking, and microfilm formation) or being intracellularly digested (e.g., toxin release, intracellular growth, and digestional resistance) [3,4,5]. Recent studies have reported diverse bacterial species and strains are resistant to digestion by protistan predators [6,7,8]. The molecular mechanisms of these bacteria-protist interactions have not been well understood, and the physiological response of protists to bacterial preys of different digestibility remains largely unknown
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