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Quantifying oxygen management and temperature and light dependencies of nitrogen fixation by Crocosphaera watsonii (2020)

Inomura, Keisuke ; Deutsch, Curtis A. ; Wilson, Samuel T. ; [et al.]

American Society for Microbiology

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Publication Date: 2022-10-26

Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Inomura, K., Deutsch, C., Wilson, S. T., Masuda, T., Lawrenz, E., Lenka, B., Sobotka, R., Gauglitz, J. M., Saito, M. A., Prášil, O., & Follows, M. J. Quantifying oxygen management and temperature and light dependencies of nitrogen fixation by Crocosphaera watsonii. Msphere, 4(6), (2019): e00531-19, doi: 10.1128/msphere.00531-19.

Description: Crocosphaera is a major dinitrogen (N2)-fixing microorganism, providing bioavailable nitrogen (N) to marine ecosystems. The N2-fixing enzyme nitrogenase is deactivated by oxygen (O2), which is abundant in marine environments. Using a cellular scale model of Crocosphaera sp. and laboratory data, we quantify the role of three O2 management strategies by Crocosphaera sp.: size adjustment, reduced O2 diffusivity, and respiratory protection. Our model predicts that Crocosphaera cells increase their size under high O2. Using transmission electron microscopy, we show that starch granules and thylakoid membranes are located near the cytoplasmic membranes, forming a barrier for O2. The model indicates a critical role for respiration in protecting the rate of N2 fixation. Moreover, the rise in respiration rates and the decline in ambient O2 with temperature strengthen this mechanism in warmer water, providing a physiological rationale for the observed niche of Crocosphaera at temperatures exceeding 20°C. Our new measurements of the sensitivity to light intensity show that the rate of N2 fixation reaches saturation at a lower light intensity (∼100 μmol m−2 s−1) than photosynthesis and that both are similarly inhibited by light intensities of 〉500 μmol m−2 s−1. This suggests an explanation for the maximum population of Crocosphaera occurring slightly below the ocean surface.

Description: We thank Stephanie Dutkiewicz and Sallie W. Chisholm for useful discussion, Martin Lukeš for technical assistance for the N2 fixation measurement, and the members of Writing and Communication Center at MIT for their advice on writing. This research was supported by the Japan Student Service Organization (JASSO) (grant L11171020001 to K.I.), the Gordon and Betty Moore Foundation (grant GBMF 3775 to C.D. and grant GBMF 3778 to M.J.F.), the U.S. National Science Foundation (grant OCE-1756524 to S.T.W., grant OCE-1558702 to M.J.F., and grant OCE-PRF 1421196 to J.M.G), the Simons Foundation (Simons Postdoctoral Fellowship in Marine Microbial Ecology award 544338 to K.I., Simons Collaboration on Ocean Processes and Ecology award 329108 to M.J.F., Simons Collaboration on Computational BIOgeochemical Modeling of Marine EcosystemS [CBIOMES] award 549931 to M.J.F.), the Czech Science Foundation (GAČR) (grant 16-15467S to O.P.), and the National Sustainability Programme (NPU) (grant LO1416 Algatech plus to O.P.).

Keywords: Crocosphaera ; Carbon ; Cell flux model ; Daily cycle ; Iron ; Light ; Nitrogen ; Nitrogen fixation ; Oxygen ; Photosynthesis ; Temperature

Repository Name: Woods Hole Open Access Server

Type: Article

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Data-based assessment of environmental controls on global marine nitrogen fixation (2014)

Luo, Ya-Wei ; Lima, Ivan D. ; Karl, David M. ; [et al.]

Copernicus Publications on behalf of the European Geosciences Union

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Publication Date: 2022-05-26

Description: © The Author(s), 2014. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Biogeosciences 11 (2014): 691-708, doi:10.5194/bg-11-691-2014.

Description: There are a number of hypotheses concerning the environmental controls on marine nitrogen fixation (NF). Most of these hypotheses have not been assessed against direct measurements on the global scale. In this study, we use ~ 500 depth-integrated field measurements of NF covering the Pacific and Atlantic oceans to test whether the spatial variance of these measurements can be explained by the commonly hypothesized environmental controls, including measurement-based surface solar radiation, mixed layer depth, average solar radiation in the mixed layer, sea surface temperature, wind speed, surface nitrate and phosphate concentrations, surface excess phosphate (P*) concentration and subsurface minimum dissolved oxygen (in upper 500 m), as well as model-based P* convergence and atmospheric dust deposition. By conducting simple linear regression and stepwise multiple linear regression (MLR) analyses, surface solar radiation (or sea surface temperature) and subsurface minimum dissolved oxygen are identified as the predictors that explain the most spatial variance in the observed NF data, although it is unclear why the observed NF decreases when the level of subsurface minimum dissolved oxygen is higher than ~ 150 μM. Dust deposition and wind speed do not appear to influence the spatial patterns of NF on global scale. The weak correlation between the observed NF and the P* convergence and concentrations suggests that the available data currently remain insufficient to fully support the hypothesis that spatial variability in denitrification is the principal control on spatial variability in marine NF. By applying the MLR-derived equation, we estimate the global-integrated NF at 74 (error range 51–110) Tg N yr−1 in the open ocean, acknowledging that it could be substantially higher as the 15N2-assimilation method used by most of the field samples underestimates NF. More field NF samples in the Pacific and Indian oceans, particularly in the oxygen minimum zones, are needed to reduce uncertainties in our conclusion.

Description: This project was supported by the NSF Center for Microbial Oceanography: Research and Education (C-MORE) (EF-0424599), an NSF Emerging Topics in Biogeochemical Cycles grant (ETBC, AGS-1020594), and the Gordon and Betty Moore Foundation.