Dataset Information

Low-Ammonium Environment Increases the Nutrient Exchange between Diatom-Diazotroph Association Cells and Facilitates Photosynthesis and N₂ Fixation-a Mechanistic Modeling Analysis.

ABSTRACT: Diatom-diazotroph associations (DDAs) are one of the most important symbiotic dinitrogen (N₂) fixing groups in the oligotrophic ocean. Despite their capability to fix N₂, ammonium (NH₄⁺) remains a key nitrogen (N) source for DDAs, and the effect of NH₄⁺ on their metabolism remains elusive. Here, we developed a coarse-grained, cellular model of the DDA with NH₄⁺ uptake and quantified how the level of extracellular NH₄⁺ influences metabolism and nutrient exchange within the symbiosis. The model shows that, under a fixed growth rate, an increased NH₄⁺ concentration may lower the required level of N₂ fixation and photosynthesis, and decrease carbon (C) and N exchange. A low-NH₄⁺ environment leads to more C and N in nutrient exchange and more fixed N₂ to support a higher growth rate. With higher growth rates, nutrient exchange and metabolism increased. Our study shows a strong effect of NH₄⁺ on metabolic processes within DDAs, and thus highlights the importance of in situ measurement of NH₄⁺ concentrations.

SUBMITTER: Gao M

PROVIDER: S-EPMC9497195 | biostudies-literature | 2022 Sep

REPOSITORIES: biostudies-literature

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Low-Ammonium Environment Increases the Nutrient Exchange between Diatom-Diazotroph Association Cells and Facilitates Photosynthesis and N2 Fixation-a Mechanistic Modeling Analysis.

Gao Meng M Armin Gabrielle G Inomura Keisuke K

Cells 20220917 18

Diatom-diazotroph associations (DDAs) are one of the most important symbiotic dinitrogen (N2) fixing groups in the oligotrophic ocean. Despite their capability to fix N2, ammonium (NH4+) remains a key nitrogen (N) source for DDAs, and the effect of NH4+ on their metabolism remains elusive. Here, we developed a coarse-grained, cellular model of the DDA with NH4+ uptake and quantified how the level of extracell ...[more]

PMID: 36139486

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Project description:The dominant marine filamentous N2 fixer, Trichodesmium, conducts photosynthesis and N2 fixation during the daytime. Because N2 fixation is sensitive to O2, some previous studies suggested that spatial segregation of N2 fixation and photosynthesis is essential in Trichodesmium. However, this hypothesis conflicts with some observations where all the cells contain both photosystems and the N2-fixing enzyme nitrogenase. Here, we construct a systematic model simulating Trichodesmium metabolism, showing that the hypothetical spatial segregation is probably useless in increasing the Trichodesmium growth and N2 fixation, unless substances can efficiently transfer among cells with low loss to the environment. The model suggests that Trichodesmium accumulates fixed carbon in the morning and uses that in respiratory protection to reduce intracellular O2 during the mid-daytime, when photosynthesis is downregulated, allowing the occurrence of N2 fixation. A cell membrane barrier against O2 and alternative non-O2 evolving electron transfer also contribute to maintaining low intracellular O2. Our study provides a mechanism enabling N2 fixation despite the presence of photosynthesis across Trichodesmium. IMPORTANCE The filamentous Trichodesmium is a globally prominent marine nitrogen fixer. A long-standing paradox is that the nitrogen-fixing enzyme nitrogenase is sensitive to oxygen, but Trichodesmium conducts both nitrogen fixation and oxygen-evolving photosynthesis during the daytime. Previous studies using immunoassays reported that nitrogenase was limited in some specialized Trichodesmium cells (termed diazocytes), suggesting the necessity of spatial segregation of nitrogen fixation and photosynthesis. However, attempts using other methods failed to find diazocytes in Trichodesmium, causing controversy on the existence of the spatial segregation. Here, our physiological model shows that Trichodesmium can maintain low intracellular O2 in mid-daytime and achieve feasible nitrogen fixation and growth rates even without the spatial segregation, while the hypothetical spatial segregation might not be useful if substantial loss of substances to the environment occurs when they transfer among the Trichodesmium cells. Our study then suggests a possible mechanism by which Trichodesmium can survive without the spatial segregation.

Dataset Information

Low-Ammonium Environment Increases the Nutrient Exchange between Diatom-Diazotroph Association Cells and Facilitates Photosynthesis and N₂ Fixation-a Mechanistic Modeling Analysis.

Publications

Low-Ammonium Environment Increases the Nutrient Exchange between Diatom-Diazotroph Association Cells and Facilitates Photosynthesis and N<sub>2</sub> Fixation-a Mechanistic Modeling Analysis.

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