Glock Nicolaas, Roy Alexandra-Sophie, Romero Dennis, Wein Tanita, Weissenbach Julia, Revsbech Niels Peter, Høgslund Signe, Clemens David, Sommer Stefan, Dagan Tal
Marine Geosystems, GEOMAR Helmholtz Centre for Ocean Research Kiel, 24148 Kiel, Germany;
Institute of Microbiology, Kiel University, 24118 Kiel, Germany.
Proc Natl Acad Sci U S A. 2019 Feb 19;116(8):2860-2865. doi: 10.1073/pnas.1813887116. Epub 2019 Feb 6.
Benthic foraminifera populate a diverse range of marine habitats. Their ability to use alternative electron acceptors-nitrate (NO) or oxygen (O)-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 O respiration rates for 10 benthic foraminifer species sampled in the Peruvian oxygen minimum zone (OMZ). Denitrification and O respiration rates significantly scale sublinearly with the cell volume. The scaling is lower for O respiration than for denitrification, indicating that NO metabolism during denitrification is more efficient than O metabolism during aerobic respiration in foraminifera from the Peruvian OMZ. The negative correlation of the O respiration rate with the surface/volume ratio is steeper than for the denitrification rate. This is likely explained by the presence of an intracellular NO storage in denitrifying foraminifera. Furthermore, we observe an increasing mean cell volume of the Peruvian foraminifera, under higher NO availability. This suggests that the cell size of denitrifying foraminifera is not limited by O but rather by NO 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 NO is the preferred electron acceptor in foraminifera from the OMZ, where the foraminiferal contribution to denitrification is governed by the ratio between NO and O.
底栖有孔虫分布于多种多样的海洋栖息地。它们能够利用替代电子受体——硝酸盐(NO)或氧气(O),这使它们成为底栖氮循环的重要调节者。然而,两种替代呼吸途径的代谢标度以及有孔虫反硝化速率的环境决定因素仍不为人所知。我们测量了在秘鲁低氧区(OMZ)采集的10种底栖有孔虫物种的反硝化和O呼吸速率。反硝化和O呼吸速率与细胞体积呈显著的亚线性标度关系。O呼吸的标度低于反硝化,这表明在来自秘鲁OMZ的有孔虫中,反硝化过程中的NO代谢比有氧呼吸过程中的O代谢更有效。O呼吸速率与表面积/体积比的负相关性比反硝化速率更陡峭。这可能是由于反硝化有孔虫中存在细胞内NO储存。此外,我们观察到在更高的NO可利用性条件下,秘鲁有孔虫的平均细胞体积增加。这表明反硝化有孔虫的细胞大小不受O的限制,而是受NO可利用性的限制。基于我们的研究结果,我们开发了一种有孔虫细胞体积的数学公式,作为呼吸和反硝化速率的预测指标,这可以进一步在生物地球化学模型中限制有孔虫的生物地球化学循环。我们的研究结果表明,在OMZ的有孔虫中,NO是首选的电子受体,其中有孔虫对反硝化的贡献受NO与O之间的比例控制。