Foraminifera are a group of amoeboid protists commonly found in various marine habitats. Several benthic foraminiferal species are known to store nitrate and use it for complete denitrification, a unique energy metabolism among eukaryotes. This property and their high density in sediments of oxygen-depleted zones, pinpoint them as important players in the oceanic nitrogen cycle. Recent estimates of the foraminiferal contribution to the total benthic denitrification in the OMZ reach up to 100%; and thus are important to constrain the biologically available nitrogen in coastal water. The mechanisms of foraminiferal denitrification are however still unknown and a contribution of associated bacteria is discussed. Here we present evidence for a novel eukaryotic denitrification pathway that is encoded in the foraminifera genomes. The presence of a denitrification pathway in ten Peruvian species thriving in oxygen minimum zones and two further species populating oxygen-depleted environments in Sweden was revealed by a large-scale sequencing of genomes and transcriptomes. These pathways include the enzymes nitrite reductase (NirK) and nitric oxide reductase (Nor) as well as a wide range of nitrite/nitrate transporters (Nrt). Furthermore, we uncovered evidence for a prokaryotic origin of the foraminiferal denitrification pathway and an ancient emergence of this trait via phylogenetic reconstruction. We propose a model for foraminiferal denitrification where a common electron transport chain is used for anaerobic and aerobic respiration. The evolution of hybrid respiration in foraminifera likely contributed to their ecological success that is well documented in paleontological records since the Cambrian.
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