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

Authors :
Christian Woehle
Alexandra-Sophie Roy
Nicolaas Glock
Jan Michels
Tanita Wein
Julia Weissenbach
Dennis Romero
Claas Hiebenthal
Stanislav N. Gorb
Joachim Schönfeld
Tal Dagan
Publication Year :
2022
Publisher :
National Academy of Sciences, 2022.

Abstract

Significance A substantial component of the global nitrogen cycle is the production of biologically inaccessible dinitrogen attributed to anaerobic denitrification by prokaryotes. Recent evidence identified a eukaryote, foraminifera, as new key players in this “loss” of bioavailable nitrogen. The evolution of denitrification in eukaryotes is a rare event, and the genetic mechanisms of the denitrification pathway in foraminifera are just starting to be elucidated. We present large-scale sequencing analyses of 10 denitrifying foraminiferal species, which reveals the high conservation of the foraminiferal denitrification pathway. We further find evidence for a complementation of denitrification by the foraminiferal microbiome. Together, these findings provide insights into the early evolution of a previously overlooked component in the marine nitrogen cycle. 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 origin. However, the prevalence of denitrification genes in foraminifera remains unknown, and the missing denitrification pathway components are elusive. Analyzing transcriptomes and metagenomes of 10 foraminiferal species from the Peruvian oxygen minimum zone, we show that denitrification genes are highly conserved in foraminifera. We infer the last common ancestor of denitrifying foraminifera, which enables us to predict the ability to denitrify for additional foraminiferal species. Additionally, an examination of the foraminiferal microbiota reveals evidence for a stable interaction with Desulfobacteraceae, which harbor genes that complement the foraminiferal denitrification pathway. Our results provide evidence that foraminiferal denitrification is complemented by the foraminifera-associated microbiome. The interaction of foraminifera with their resident bacteria is at the basis of foraminiferal adaptation to anaerobic environments that manifested in ecological success in oxygen depleted habitats.

Details

Language :
English
Database :
OpenAIRE
Accession number :
edsair.doi.dedup.....f099c9a931077532e9cb61d42bca15da
Full Text :
https://doi.org/10.1073/pnas.2200198119