Abstract
Grazing by heterotrophic protists influences plankton population dynamics, community composition, and the flux of carbon through marine planktonic food webs. To gain insight into the molecular underpinnings of grazing in dinoflagellates, a group of important heterotrophic protists, we used an RNA-seq approach to investigate the transcriptomic response of Oxyrrhis marina under fed and starved treatments with three different phytoplankton prey (Isochrysis galbana and two strains of Heterosigma akashiwo). In response to fed and starved conditions, 1,575 transcripts were significantly differentially expressed in O. marina. Fed O. marina cells upregulated transcripts involved in the synthesis of essential fatty acids and storage carbohydrates suggesting that the predator was food satiated and excess glucose was being stored as an energy reserve. Transcripts encoding voltage-gated ion channels were also upregulated during grazing, and they are known to be involved in the detection of mechanical stimuli and the regulation of swimming behavior in several eukaryotic protists. Fed O. marina cells upregulated kinases, which can dictate cell shape changes and may be associated with phagocytosis. During starvation, upregulated O. marina transcripts included those involved in the degradation of energy-storage molecules like glucan 1,4 alpha-glycosidase and those involved in antioxidant activities and autophagy, like acid ceramidase that are associated with the digestion of polar lipids present in cell membranes. Starved O. marina also upregulated transcripts with high similarity to proton pumping proteorodopsins suggesting that this heterotrophic protist may supplement its energy requirement during starvation with a light harvesting mechanism. Although herbivorous grazing is a pivotal transformation in the C cycle, logistical constraints limit our investigations of environmental and biological drivers. The molecular signals identified here provide new insights into the metabolic regulation of feeding and starvation in marine heterotrophic protists and can fuel hypothesis-driven research into predators' metabolic response to prey availability.
Highlights
Grazing by unicellular eukaryotic herbivorous marine plankton on phytoplankton constitutes the single largest loss process of primary production in the marine environment and is important in mediating plankton population dynamics and community composition, and the flow of energy and material throughout marine planktonic food webs (Tillmann, 2004; Schmoker et al, 2013; Weisse et al, 2016)
Evidence of active grazing was observed in the rapid decrease of prey from between 1.28 × 104 and 2 × 105 cells ml−1 at the start of the experiment, to below 103 cells ml−1 after 3 days
The abundance of I. galbana in the fed treatment was very low on day 3 and was not detectable using our counting methods; the concentration was conservatively estimated at
Summary
Grazing by unicellular eukaryotic herbivorous marine plankton (i.e., microzooplankton, heterotrophic protists) on phytoplankton constitutes the single largest loss process of primary production in the marine environment and is important in mediating plankton population dynamics and community composition, and the flow of energy and material throughout marine planktonic food webs (Tillmann, 2004; Schmoker et al, 2013; Weisse et al, 2016). Heterotrophic protists are the main consumers of marine phytoplankton biomass, consuming on average over 60% of daily phytoplankton production (Calbet and Landry, 2004). These herbivores are important prey for larger zooplankton and serve as important trophic links in marine food webs (Calbet and Saiz, 2005; Campbell et al, 2009; Löder et al, 2011). The population dynamics of marine plankton are disproportionately affected by heterotrophic protists, because these predators have growth rates that can equal or exceed the growth rates of their phytoplankton prey (Hansen et al, 1997). Despite the key importance of heterotrophic protists in marine food webs and global biogeochemical processes, considerable knowledge gaps persist in understanding the metabolic processes involved in protistan herbivory
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