Literature DB >> 30728294

Metabolic preference of nitrate over oxygen as an electron acceptor in foraminifera from the Peruvian oxygen minimum zone.

Nicolaas Glock1, Alexandra-Sophie Roy2, Dennis Romero3, Tanita Wein2, Julia Weissenbach2, Niels Peter Revsbech4, Signe Høgslund5, David Clemens6, Stefan Sommer6, Tal Dagan2.   

Abstract

Benthic foraminifera populate a diverse range of marine habitats. Their ability to use alternative electron acceptors-nitrate (NO3 -) or oxygen (O2)-makes them important mediators of benthic nitrogen cycling. Nevertheless, the metabolic scaling of the two alternative respiration pathways and the environmental determinants of foraminiferal denitrification rates are yet unknown. We measured denitrification and O2 respiration rates for 10 benthic foraminifer species sampled in the Peruvian oxygen minimum zone (OMZ). Denitrification and O2 respiration rates significantly scale sublinearly with the cell volume. The scaling is lower for O2 respiration than for denitrification, indicating that NO3 - metabolism during denitrification is more efficient than O2 metabolism during aerobic respiration in foraminifera from the Peruvian OMZ. The negative correlation of the O2 respiration rate with the surface/volume ratio is steeper than for the denitrification rate. This is likely explained by the presence of an intracellular NO3 - storage in denitrifying foraminifera. Furthermore, we observe an increasing mean cell volume of the Peruvian foraminifera, under higher NO3 - availability. This suggests that the cell size of denitrifying foraminifera is not limited by O2 but rather by NO3 - availability. Based on our findings, we develop a mathematical formulation of foraminiferal cell volume as a predictor of respiration and denitrification rates, which can further constrain foraminiferal biogeochemical cycling in biogeochemical models. Our findings show that NO3 - is the preferred electron acceptor in foraminifera from the OMZ, where the foraminiferal contribution to denitrification is governed by the ratio between NO3 - and O2.

Entities:  

Keywords:  eukaryotic denitrification; foraminifera; nitrogen cycle; oxygen minimum zone

Year:  2019        PMID: 30728294      PMCID: PMC6386669          DOI: 10.1073/pnas.1813887116

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  18 in total

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Journal:  Nature       Date:  2005-09-15       Impact factor: 49.962

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Journal:  Nature       Date:  2003-04-10       Impact factor: 49.962

3.  Denitrification likely catalyzed by endobionts in an allogromiid foraminifer.

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Journal:  ISME J       Date:  2011-12-01       Impact factor: 10.302

4.  Diatoms respire nitrate to survive dark and anoxic conditions.

Authors:  Anja Kamp; Dirk de Beer; Jana L Nitsch; Gaute Lavik; Peter Stief
Journal:  Proc Natl Acad Sci U S A       Date:  2011-03-14       Impact factor: 11.205

5.  Production of N(2) through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments.

Authors:  Bo Thamdrup; Tage Dalsgaard
Journal:  Appl Environ Microbiol       Date:  2002-03       Impact factor: 4.792

6.  Expanding oxygen-minimum zones in the tropical oceans.

Authors:  Lothar Stramma; Gregory C Johnson; Janet Sprintall; Volker Mohrholz
Journal:  Science       Date:  2008-05-02       Impact factor: 47.728

7.  Denitrification by the fungus Cylindrocarpon tonkinense: anaerobic cell growth and two isozyme forms of cytochrome P-450nor.

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Journal:  Appl Environ Microbiol       Date:  1995-03       Impact factor: 4.792

8.  Anaerobic oxidation of ammonium is a biologically mediated process.

Authors:  A A van de Graaf; A Mulder; P de Bruijn; M S Jetten; L A Robertson; J G Kuenen
Journal:  Appl Environ Microbiol       Date:  1995-04       Impact factor: 4.792

9.  Coupling of oceanic carbon and nitrogen facilitates spatially resolved quantitative reconstruction of nitrate inventories.

Authors:  Nicolaas Glock; Zeynep Erdem; Klaus Wallmann; Christopher J Somes; Volker Liebetrau; Joachim Schönfeld; Stanislav Gorb; Anton Eisenhauer
Journal:  Nat Commun       Date:  2018-03-23       Impact factor: 14.919

10.  A Novel Eukaryotic Denitrification Pathway in Foraminifera.

Authors:  Christian Woehle; Alexandra-Sophie Roy; Nicolaas Glock; Tanita Wein; Julia Weissenbach; Philip Rosenstiel; Claas Hiebenthal; Jan Michels; Joachim Schönfeld; Tal Dagan
Journal:  Curr Biol       Date:  2018-08-02       Impact factor: 10.834

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  8 in total

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

Authors:  Christian Woehle; Alexandra-Sophie Roy; Nicolaas Glock; Jan Michels; Tanita Wein; Julia Weissenbach; Dennis Romero; Claas Hiebenthal; Stanislav N Gorb; Joachim Schönfeld; Tal Dagan
Journal:  Proc Natl Acad Sci U S A       Date:  2022-06-15       Impact factor: 12.779

2.  Diversity hotspot and unique community structure of foraminifera in the world's deepest marine blue hole - Sansha Yongle Blue Hole.

Authors:  Qingxia Li; Yanli Lei; Raphaёl Morard; Tiegang Li; Baodong Wang
Journal:  Sci Rep       Date:  2020-06-24       Impact factor: 4.379

3.  Anaerobic metabolism of Foraminifera thriving below the seafloor.

Authors:  William D Orsi; Raphaël Morard; Aurele Vuillemin; Michael Eitel; Gert Wörheide; Jana Milucka; Michal Kucera
Journal:  ISME J       Date:  2020-07-08       Impact factor: 10.302

4.  Effects of temperature on the behaviour and metabolism of an intertidal foraminifera and consequences for benthic ecosystem functioning.

Authors:  Noémie Deldicq; Dewi Langlet; Camille Delaeter; Grégory Beaugrand; Laurent Seuront; Vincent M P Bouchet
Journal:  Sci Rep       Date:  2021-02-17       Impact factor: 4.379

5.  Heterotrophic Foraminifera Capable of Inorganic Nitrogen Assimilation.

Authors:  Clare Bird; Charlotte LeKieffre; Thierry Jauffrais; Anders Meibom; Emmanuelle Geslin; Helena L Filipsson; Olivier Maire; Ann D Russell; Jennifer S Fehrenbacher
Journal:  Front Microbiol       Date:  2020-12-03       Impact factor: 5.640

6.  Multiple integrated metabolic strategies allow foraminiferan protists to thrive in anoxic marine sediments.

Authors:  Fatma Gomaa; Daniel R Utter; Christopher Powers; David J Beaudoin; Virginia P Edgcomb; Helena L Filipsson; Colleen M Hansel; Scott D Wankel; Ying Zhang; Joan M Bernhard
Journal:  Sci Adv       Date:  2021-05-26       Impact factor: 14.136

7.  Kleptoplast distribution, photosynthetic efficiency and sequestration mechanisms in intertidal benthic foraminifera.

Authors:  Bruno Jesus; Thierry Jauffrais; Erik C L Trampe; Johannes W Goessling; Charlotte Lekieffre; Anders Meibom; Michael Kühl; Emmanuelle Geslin
Journal:  ISME J       Date:  2021-10-11       Impact factor: 10.302

8.  Abundant Chitinous Structures in Chilostomella (Foraminifera, Rhizaria) and Their Potential Functions.

Authors:  Hidetaka Nomaki; Chong Chen; Kaya Oda; Masashi Tsuchiya; Akihiro Tame; Katsuyuki Uematsu; Noriyuki Isobe
Journal:  J Eukaryot Microbiol       Date:  2020-11-20       Impact factor: 3.346

  8 in total

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