Denitrification in foraminifera has ancient origin and is complemented by associated bacteria

Abstract

Benthic foraminifera are unicellular eukaryotes that inhabit sediments of aquatic environments. Several foraminifera of the order Rotaliida are known to store and use nitrate for denitrification, a unique energy metabolism among eukaryotes. The rotaliid Globobulimina spp. has been shown to encode an incomplete denitrification pathway of bacterial origins. However, the prevalence of denitrification genes in foraminifera remains unknown and the missing denitrification pathway components are elusive. Analysing transcriptomes and metagenomes of ten foraminifera species from the Peruvian oxygen minimum zone, we show that denitrification genes are highly conserved in foraminifera. We infer of the last common ancestor of denitrifying foraminifera, which enables us to predict further denitrifying species. Additionally, an examination of the foraminifera microbiota reveals evidence for a stable interaction with Desulfobacteracea, which harbour genes that complement the foraminifera denitrification pathway. Our results provide evidence that foraminiferal denitrification is complemented by the foraminifera microbiome. The interaction of Foraminifera with their resident bacteria is at the basis of foraminifera adaptation to anaerobic environments that manifested in ecological success within oxygen depleted habitats.