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

Christian Woehle, Alexandra Sophie Roy, Nicolaas Glock, Jan Michels, Tanita Wein, Julia Weissenbach, Dennis Romero, Claas Hiebenthal, Stanislav N. Gorb, Joachim Schonfeld, Tal Dagan

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish
Article numbere2200198119
Number of pages11
JournalProceedings of the National Academy of Sciences
Volume119
Issue number25
DOIs
StatePublished - 21 Jun 2022
Externally publishedYes

Keywords

  • denitrification
  • evolution
  • foraminifera
  • genomics
  • microbiome

All Science Journal Classification (ASJC) codes

  • General

Fingerprint

Dive into the research topics of 'Denitrification in foraminifera has an ancient origin and is complemented by associated bacteria'. Together they form a unique fingerprint.

Cite this