All in a day's work: feeding, digestion and carbon transformation by microzooplankton

Microzooplankton are the main consumers of phytoplankton biomass in the ocean, consuming on average >60% of daily phytoplankton production. Microzooplankton feeding activities influence phytoplankton abundance, size spectrum, species composition and potential for export production. 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 microzooplankton grazing. Here, we describe the metabolic response to prey availability in a suite of three phylogenetically distinct heterotrophic dinoflagellates, an important group of microzooplankton, using a combination of metatranscriptomes, laboratory experiments, grazing rate measurements and physiological assays. The metabolic response to food availability included key aspects of the feeding and digestion process such as the upregulation of voltage-gated ion channels, which are known to be involved in the detection of mechanical stimuli and the regulation of swimming behavior in several eukaryotic protists. We also identified the upregulation of both phagosomal proteins associated with phagosome formation and prey capture and lysosomal enzymes involved in particle digestion. Our biochemical measurements revealed that grazing and growth rates in the presence of prey differed among species, as did mortality in the absence of prey. Interestingly, the timing of gene transcription involved in ingestion and digestion differed among species. Together these results suggest that dinoflagellate species may parse ingestion and digestion in different ways, providing a mechanism for how microzooplankton community composition and their activities may impact nutrient regeneration and carbon cycling in the ocean.