Gene expression in the mixotrophic prymnesiophyte, Prymnesium parvum, responds to prey availability

Abstract

The mixotrophic prymnesiophyte, Prymnesium parvum, is a widely distributed alga with significant ecological importance. It produces toxins and can form ecosystem disruptive blooms that result in fish kills and changes in planktonic food web structure. However, the relationship between P. parvum and its prey on the molecular level is poorly understood. In this study, we used RNA-Seq technology to study changes in gene transcription of P. parvum in three treatments with different microbial populations available as potential prey: axenic P. parvum (no prey), bacterized P. paruvm, and axenic P. parvum with ciliates added as prey. Thousands of genes were differentially expressed among the three treatments. Most notably, transcriptome data indicated that P. parvum obtained organic carbon, including fatty acids, from both bacteria and ciliate prey for energy and cellular building blocks. The data also suggested that different prey provided P. parvum with macro- and micro-nutrients, namely organic nitrogen in the form of amino acids from ciliates, and iron from bacteria. However, both transcriptomic data and growth experiments indicated that P. parvum did not grow faster in the presence of prey despite the gains in nutrients, although algal abundances attained in culture were slightly greater in the presence of prey. The relationship between phototrophy, heterotrophy and growth of P. parvum is discussed.

Transcriptomic Response to Feeding and Starvation in a Herbivorous Dinoflagellate

“…These data provide insights into the molecular underpinnings of the feeding and starvation processes. We found 3.4% of the transcriptome (1576 O. marina contigs) to be regulated on the transcriptional level which is in general agreement with other dinoflagellates (reviewed by Roy et al, 2018) and other eukaryotic organisms (e.g., Dyhrman et al, 2012;Bochenek et al, 2013;Liu et al, 2015). Here, the transcriptomic response of the predator feeding on high prey concentrations included 972 upregulated transcripts revealing cellular and metabolic processes indicative of active grazing.…”

“…Interestingly, a comparison of gene content in a mixotrophic alga and a heterotroph (both ciliates) did not reveal significant differences in gene content in relation to trophic mode (Santoferrara et al, 2014). One study that examined differentially expressed genes and thus potential metabolic differences in feeding status focused on a mixotrophic alga either feeding on prey or photosynthesizing (Liu et al, 2015). Differentially expressed genes in that study were associated primarily with preyderived nutrient uptake, such as iron from bacterial prey and organic nitrogen from ciliate prey.…”

Comparative Transcriptomics Reveals Distinct Gene Expressions of a Model Ciliated Protozoan Feeding on Bacteria-Free Medium, Digestible, and Digestion-Resistant Bacteria

“…This observation in the heterotrophic protist is different from previous findings for a mixotrophic alga Ochromonas, which had upregulated expression of the genes encoding for unidirectional enzymes GCK and PFK, implying a higher glycolytic activity when feeding on a bacteria prey [15]. A mixotrophic haptophyte Prymnesium parvum feeding on bacteria and ciliates also exhibited upregulation of the genes involved in TCA and the glyoxylate cycle [16]. These contradictory results for the heterotrophic Tetrahymena and the mixotrophs might be related to their different trophic lifestyles.…”

“…Transcriptomic analysis has increasingly been exploited as a high throughput approach to understand the physiological and molecular responses of microbial eukaryotes to environmental factors and to identify the genes that are associated with specific nutritional strategies [13]. Using a transcriptomic approach, some phototrophic or mixotrophic algae (e.g., diatoms and dinoflagellates) have been studied, demonstrating specific genes involving biochemical synthesis, fatty acid oxidation, TCA cycle, nitrogen and/or iron uptakes were up-and downregulated in response to the presence of bacterial preys [14][15][16][17]. Knowledge of the metabolic processes involved in heterotrophic nutrition has been gleaned mostly from a few transcriptomic studies focused on identifying the genes involved in phagocytosis, e.g., in prey recognition, transcription regulation, and phagosomal membrane formation, as revealed in the slime mold Dictyostelium discoideum [18].…”

Acknowledging and incorporating mixed nutrition into aquatic protistan ecology, finally

“…Genetic approaches to answer these questions are at the forefront. Such studies are identifying changes in gene expression that accompany shifts in the nutritional mode of mixotrophic algae (Liu et al ., ), transcriptional activity of chloroplasts in kleptoplastidic ciliates (Johnson et al ., ), and the molecular signaling that takes place between heterotrophic hosts and symbiotic algae in the establishment of mutualistic associations (Balzano et al ., ). At present, such applications make use primarily of transcriptomics because of the daunting size of eukaryotic genomes, but genome sequencing of microbial eukaryotes (including mixotrophic species) is rapidly becoming economically feasible.…”