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- Woehle, Christian, et al.
(author)
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A Novel Eukaryotic Denitrification Pathway in Foraminifera
- 2018
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In: Current Biology. - : Cell Press. - 0960-9822 .- 1879-0445. ; 28:16, s. 2536-2543.e5
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Journal article (peer-reviewed)abstract
- Benthic foraminifera are unicellular eukaryotes inhabiting sediments of aquatic environments. Several species were shown to store and use nitrate for complete denitrification, a unique energy metabolism among eukaryotes. The population of benthic foraminifera reaches high densities in oxygen-depleted marine habitats, where they play a key role in the marine nitrogen cycle. However, the mechanisms of denitrification in foraminifera are still unknown, and the possibility of a contribution of associated bacteria is debated. Here, we present evidence for a novel eukaryotic denitrification pathway that is encoded in foraminiferal genomes. Large-scale genome and transcriptomes analyses reveal the presence of a denitrification pathway in foraminifera species of the genus Globobulimina. This includes the enzymes nitrite reductase (NirK) and nitric oxide reductase (Nor) as well as a wide range of nitrate transporters (Nrt). A phylogenetic reconstruction of the enzymes’ evolutionary history uncovers evidence for an ancient acquisition of the foraminiferal denitrification pathway from prokaryotes. We propose a model for denitrification in foraminifera, 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, which is well documented in palaeontological records since the Cambrian period. Woehle, Roy, et al. report a novel eukaryotic denitrification pathway in foraminiferal genomes. The enzymes nitrite reductase (NirK) and nitric oxide reductase (Nor) are encoded in Globobulimina. A phylogenetic analysis provides insights into the genetic capacity for denitrification in foraminifera and its evolutionary origin in prokaryotes.
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| 2. |
- Woehle, Christian, et al.
(author)
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Denitrification in foraminifera has an ancient origin and is complemented by associated bacteria
- 2022
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In: Proceedings of the National Academy of Sciences of the United States of America. - : National Academy of Science. - 0027-8424 .- 1091-6490. ; 119:25
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Journal article (peer-reviewed)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.
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