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Metabolic Preference of Nitrate Over Oxygen As an Electron Acceptor in Foraminifera from the Peruvian Oxygen Minimum Zone

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Metabolic Preference of Nitrate Over Oxygen As an Electron Acceptor in Foraminifera from the Peruvian Oxygen Minimum Zone Metabolic preference of nitrate over oxygen as an electron acceptor in foraminifera from the Peruvian oxygen minimum zone Nicolaas Glocka,1, Alexandra-Sophie Royb, Dennis Romeroc, Tanita Weinb, Julia Weissenbachb,2, Niels Peter Revsbechd, Signe Høgslunde, David Clemensa, Stefan Sommera, and Tal Daganb aMarine Geosystems, GEOMAR Helmholtz Centre for Ocean Research Kiel, 24148 Kiel, Germany; bInstitute of Microbiology, Kiel University, 24118 Kiel, Germany; cDirección General de Investigaciones Oceanográficas y Cambio Climático, Instituto del Mar del Perú, Callao 01, Peru 17; dAarhus University Centre for Water Technology, Department of Bioscience, Aarhus University, DK-8000 Aarhus C, Denmark; and eSection of Marine Ecology, Department of Bioscience, Aarhus University, DK-8000 Aarhus C, Denmark Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved January 4, 2019 (received for review August 11, 2018) Benthic foraminifera populate a diverse range of marine habitats. endobionts in some groomiid and allogromiid species (16, 17), some − Their ability to use alternative electron acceptors—nitrate (NO3 )or rotaliids surely have an eukaryotic denitrification pathway (18, 19). oxygen (O2)—makes them important mediators of benthic nitrogen A recent study of the enzymes involved in the foraminiferal de- cycling. Nevertheless, the metabolic scaling of the two alternative nitrification pathway in rotaliids showed that they are of an ancient − respiration pathways and the environmental determinants of fora- prokaryotic origin (19). The uptake of NO3 and O2 in foraminifera is likely facilitated by the pores present in the foraminiferal tests, miniferal denitrification rates are yet unknown. We measured de- − nitrification and O2 respiration rates for 10 benthic foraminifer whereas the pore density can be used as a quantitative NO3 proxy species sampled in the Peruvian oxygen minimum zone (OMZ). De- [e.g., in Bolivina spissa (20–22)]. Recent studies estimated that fo- nitrification and O2 respiration rates significantly scale sublinearly raminifera account for a major part of benthic denitrification in OMZs due to their high abundance in those habitats and their with the cell volume. The scaling is lower for O2 respiration than for − − contribution to biological NO transport (11, 23, 24). In the denitrification, indicating that NO3 metabolism during denitrifica- 3 Peruvian OMZ, foraminifera and sulfur bacteria that perform tion is more efficient than O2 metabolism during aerobic respiration − EARTH, ATMOSPHERIC, DNRA compete for the available NO (23–25). The latter process AND PLANETARY SCIENCES in foraminifera from the Peruvian OMZ. The negative correlation of + 3 produces NH4 that feeds the environment with reactive N. The the O2 respiration rate with the surface/volume ratio is steeper than + for the denitrification rate. This is likely explained by the presence NH4 can subsequently be removed by anammox either by benthic − endosymbiotic bacteria or in the water column (26, 27). Anammox of an intracellular NO3 storage in denitrifying foraminifera. Fur- thermore, we observe an increasing mean cell volume of the Peru- appears to be the main pelagic sink for dissolved reactive N in the − vian foraminifera, under higher NO availability. This suggests that Peruvian OMZ (28). These complex interactions pinpoint the im- 3 portance of benthic foraminiferal denitrification for the global N the cell size of denitrifying foraminifera is not limited by O2 but PHYSIOLOGY rather by NO − availability. Based on our findings, we develop a cycling. Nevertheless, species-specific foraminiferal denitrification 3 rates are very scarce in the literature and the measured rates vary mathematical formulation of foraminiferal cell volume as a predic- – tor of respiration and denitrification rates, which can further con- by one to two orders of magnitude (9 11, 29, 30). Equally less is known about foraminiferal O respiration rates (11, 31–38). Thus, strain foraminiferal biogeochemical cycling in biogeochemical 2 − models. Our findings show that NO3 is the preferred electron ac- ceptor in foraminifera from the OMZ, where the foraminiferal con- Significance − tribution to denitrification is governed by the ratio between NO3 and O2. Foraminifera are able to respire nitrate instead of oxygen, a rare ability amongst eukaryotes. Here, we show that benthic forami- eukaryotic denitrification | foraminifera | oxygen minimum zone | nifera from the Peruvian oxygen minimum zone are not just nitrogen cycle facultative anaerobes by switching to nitrate respiration when oxygen is depleted but that denitrification is their preferred res- ioavailable nitrogen (N) is an essential building block of piration pathway. Their metabolic adaptations allow some spe- Bamino and nucleic acids in all living organisms (1). Nitrate cies to grow larger than predicted by cell physiology of aerobic − (NO ) is the most abundant form of reactive inorganic N within organisms due to oxygen limitation. Finally, we formulate, from 3 our observations, mathematical equations to predict the amount the oceans and a limiting nutrient for primary productivity within of foraminiferal denitrification using their cell volume. Nitrate is the surface ocean (2–4). The two main sinks for bioavailable N an important macronutrient, and denitrification is the main oce- within the oceans are heterotrophic denitrification (i.e., the re- − anic nitrate sink. Our equations will help to constrain bio- duction of NO3 to N2 during organic matter degradation) and + geochemical models for marine nitrate cycling. anaerobic ammonium (NH4 ) oxidation (anammox) (5–7). About 20–40% of the oceanic N loss takes place in oxygen Author contributions: N.G., A.-S.R., N.P.R., S.H., and T.D. designed research; N.G., A.-S.R., minimum zones (OMZs), making them key regions for global D.R., T.W., J.W., D.C., S.S., and T.D. performed research; N.P.R. contributed new reagents/ oceanic nutrient cycling (2, 4, 8). analytic tools; N.G., D.C., and S.S. analyzed data; and N.G. wrote the paper. − The authors declare no conflict of interest. Benthic foraminifera are able to use NO3 as an electron acceptor for denitrification, which is a rare ability among eukaryotes (9–11). This article is a PNAS Direct Submission. The only other eukaryotes known to date to perform incomplete Published under the PNAS license. − denitrification of NO3 are two fungi (12) and the protist Loxodes 1To whom correspondence should be addressed. Email: [email protected]. − (13). Additional eukaryotes that are able to use NO3 as an electron 2 – − Present address: Faculty of Biology, Technion Israel Institute of Technology, 320000 acceptor are two diatom species, which perform dissimilatory NO3 Haifa, Israel. + reduction to NH4 (DNRA) (14, 15). Notably, benthic foraminifera This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. are the only eukaryotes known to perform complete denitrification 1073/pnas.1813887116/-/DCSupplemental. to N2 gas (9, 15). While denitrification seems to be performed by www.pnas.org/cgi/doi/10.1073/pnas.1813887116 PNAS Latest Articles | 1of6 Downloaded by guest on September 27, 2021 additional rate measurements are crucial to calculate sound esti- A ) 5000 B. seminuda C. limbataauka B. costata mates for the total benthic foraminiferal denitrification rates and -1 N. auris B. spissa U. striata to constrain the role of foraminifera in benthic O2 respiration and day B. plicata C. carmenensis V. inflata carbon degradation. -1 all Pot.Fit (all) ind Various characteristics of organisms, from energy consumption to 500 population growth rate, are known to correlate with body size (39). ln(y) = 0.68.ln(x) - 5.57 The scaling of these characteristics with body size is well described R2 = 0.49; F = 30.1 by a power function with a scaling exponent α (39). The function is n = 33; P = 5.3E-6 considered superlinear if α > 1, linear if α = 1 and sublinear if α < 1. 50 According to “Kleiber’slaw,” the scaling of metabolic rates with bodysizeinmammalsandbirdsissublinear(α = 0.75) (40). Nonetheless, recent studies showed that the scaling of metabolic 5 rates with body size varies among different taxa. Metabolic scaling is rate (pmol Denitrification 1.0E+05 1.0E+06 1.0E+07 1.0E+08 superlinear in prokaryotes, linear in protists, and sublinear in Cell volume (µm3) α B ) metazoans (39). At extremely large cell sizes, decreases for pro- -1 1.E-03 karyotes and protists, leading to an overlap between large pro- B. seminuda C. limbataauka B. costata day 3 N. auris B. spissa U. striata - karyotes and small protists as well as between large protists and B. plicata C. carmenensis V. inflata small metazoans. The larger classes of organisms are more efficient µm all Pot.Fit (all) and competitive at larger body sizes, because more complex re- 1.E-04 spiratory systems help to sustain higher demands for electron ac- pmol ceptors (39). Notably, the concept of metabolic scaling is useful to compare the efficiency between different metabolic pathways. Thus, when the rate of different metabolic pathways within a taxon—e.g., — 1.E-05 O2 respiration and denitrification scale with different exponents ln(y) = -0.32.ln(x) - 5.57 (α), the pathway with the larger α is considered to be more efficient. R2 = 0.18; F = 6.6 n = 33; P = 0.015 Here, we determined rates of denitrification and O2 respira- tion in benthic foraminifera from the Peruvian OMZ. We ana- 1.E-06 lyzed the relationship between these metabolic rates and the 1.0E+05 1.0E+06 1.0E+07 1.0E+08 individual cell volume and the surface to volume ratio of the rate ( Specific denitrification Cell volume (µm3) foraminifera. Finally, we tested for a metabolic preference be- Fig. 1. Log–log plots and power regressions for individual foraminiferal tween denitrification and O2 respiration in foraminifera from OMZs by comparing the metabolic scaling of the two processes. denitrification rates (A) and volume-specific foraminiferal denitrification rates (B) against cell volume for benthic foraminifera from the Peruvian OMZ. Error Results bars are SEM (1SEM).
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