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

Woehle, Christian (author)
Univ Kiel, Germany;Miltenyi Biotec BV & Co KG, Germany
Roy, Alexandra-Sophie (author)
Univ Kiel, Germany
Glock, Nicolaas (author)
GEOMAR Helmholtz Ctr Ocean Res Kiel, Germany;Univ Hamburg, Germany
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Michels, Jan (author)
Univ Kiel, Germany
Wein, Tanita (author)
Univ Kiel, Germany;Weizmann Inst Sci, Israel
Weissenbach, Julia (author)
Univ Kiel, Germany
Romero, Dennis (author)
Inst Mar Peru, Peru
Hiebenthal, Claas (author)
GEOMAR Helmholtz Ctr Ocean Res Kiel, Germany
Gorb, Stanislav N. (author)
Univ Kiel, Germany
Schoenfeld, Joachim (author)
GEOMAR Helmholtz Ctr Ocean Res Kiel, Germany
Dagan, Tal (author)
Univ Kiel, Germany
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 (creator_code:org_t)
2022-06-15
2022
English.
In: Proceedings of the National Academy of Sciences of the United States of America. - : National Academy of Science. - 0027-8424 .- 1091-6490. ; 119:25
  • Journal article (peer-reviewed)
Abstract Subject headings
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  • 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.

Subject headings

NATURVETENSKAP  -- Biologi -- Evolutionsbiologi (hsv//swe)
NATURAL SCIENCES  -- Biological Sciences -- Evolutionary Biology (hsv//eng)
NATURVETENSKAP  -- Biologi -- Mikrobiologi (hsv//swe)
NATURAL SCIENCES  -- Biological Sciences -- Microbiology (hsv//eng)
NATURVETENSKAP  -- Biologi -- Ekologi (hsv//swe)
NATURAL SCIENCES  -- Biological Sciences -- Ecology (hsv//eng)

Keyword

foraminifera
denitrification
genomics
evolution
microbiome
Evolutionary Biology
Evolutionsbiologi
Mikrobiologi
Microbiology

Publication and Content Type

ref (subject category)
art (subject category)

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