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

Woehle, Christian, Roy, Alexandra-Sophie, Glock, Nicolaas, Michels, Jan, Wein, Tanita, Weissenbach, Julia, Romero, Dennis, Hiebenthal, Claas , Gorb, Stanislav, Schönfeld, Joachim and Dagan, Tal (2022) Denitrification in foraminifera has an ancient origin and is complemented by associated bacteria. Open Access PNAS Proceedings of the National Academy of Sciences of the United States of America, 119 (25). Art.Nr. e2200198119. DOI 10.1073/pnas.2200198119.

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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.
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.

Document Type: Article
Keywords: Foraminifera; dentrification; genomics; evolution; microbiome
Research affiliation: OceanRep > GEOMAR > FB2 Marine Biogeochemistry > FB2-MG Marine Geosystems
OceanRep > The Future Ocean - Cluster of Excellence
OceanRep > SFB 754
OceanRep > GEOMAR > FB1 Ocean Circulation and Climate Dynamics > FB1-P-OZ Paleo-Oceanography
OceanRep > GEOMAR > FB3 Marine Ecology > FB3-EOE-B Experimental Ecology - Benthic Ecology
Kiel University
Main POF Topic: PT6: Marine Life
Refereed: Yes
Open Access Journal?: No
Publisher: National Academy of Sciences
Projects: SFB754, Future Ocean
Date Deposited: 10 Jan 2022 12:15
Last Modified: 08 Feb 2023 09:36

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