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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