A Novel Eukaryotic Denitrification Pathway in Foraminifera

Woehle, Christian, Roy, Alexandra-Sophie, Glock, Nicolaas, Wein, Tanita, Weissenbach, Julia, Rosenstiel, Philip, Hiebenthal, Claas, Michels, Jan, Schönfeld, Joachim and Dagan, Tal (2018) A Novel Eukaryotic Denitrification Pathway in Foraminifera Current Biology, 28 (16). 2536-2543.e5. DOI 10.1016/j.cub.2018.06.027.

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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.

Document Type: Article
Keywords: protists, foraminifera, Globobulimina, energy metabolism, denitrification, eukaryotic evolution, phylogenetics, transcriptomics, metagenomics, nitrogen cycle
Research affiliation: OceanRep > GEOMAR > FB2 Marine Biogeochemistry > FB2-MG Marine Geosystems
Kiel University > Kiel Marine Science
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
Refereed: Yes
DOI etc.: 10.1016/j.cub.2018.06.027
ISSN: 0960-9822
Projects: Future Ocean, SFB754
Date Deposited: 07 Sep 2018 08:59
Last Modified: 06 Feb 2019 10:30
URI: http://eprints.uni-kiel.de/id/eprint/44162

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