Unexpected Abundance and Gene Expression of Polarella from a Tropical Oxygen Deficient Zone

Although dinoflagellates constitute a large portion of the global planktonic biomass, relatively few studies have focused on free-living dinoflagellate species and their potential contribution to biogeochemical cycling across redox gradients. Using samples from the eastern tropical North Pacific, a large, permanently stratified oxygen deficient zone and a hotspot for biogeochemical cycling, we investigated Polarella, a dinoflagellate genus that accounted for a relatively large proportion of the total RNA pool. Despite the conventional view that Polarella and its only known species, Polarella glacialis, have a bipolar distribution, analyses of metagenomes and metatranscriptomes revealed the presence and gene expression of both the genus and species in the tropical Pacific Ocean. Differential expression analysis comparing samples from oxygenated surface waters, the oxycline, and anoxic depths revealed the upregulation of stress response genes in Polarella to cope with oxidative stress. Phototrophic genes were upregulated in the euphotic zone, including near its base, where light levels approached the threshold for phototrophy, and potentially contributed to the deep chlorophyll maximum. The upregulation of genes encoding extracellular carbohydrate-active enzymes and organic substrate transporters suggests that Polarella is potentially mixotrophic. Although the overall gene expression of Polarella was low at anoxic and disphotic depths, the upregulation of transporters for a suite of inorganic nutrients (e.g., nitrate, phosphate, iron, and molybdate) suggests an opportunistic lifestyle. Collectively, these findings suggest that Polarella thrives beyond polar regions and likely plays a more prominent ecological and biogeochemical role in the ocean than previously recognized.