Mechanistic Model for the Coexistence of Nitrogen Fixation and Photosynthesis in Marine <italic toggle="yes">Trichodesmium</italic>

ABSTRACT The cyanobacterium Trichodesmium is an important contributor of new nitrogen (N) to the surface ocean, but its strategies for protecting the nitrogenase enzyme from inhibition by oxygen (O2) remain poorly understood. We present a dynamic physiological model to evaluate hypothesized conditio...

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Autores principales:	Keisuke Inomura, Samuel T. Wilson, Curtis Deutsch
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Trichodesmium carbon nitrogen nitrogen fixation nitrogenase oxygen Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/02cc2bf524b947f98db48b55c0b6e8da
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spelling	oai:doaj.org-article:02cc2bf524b947f98db48b55c0b6e8da2021-12-02T18:25:16ZMechanistic Model for the Coexistence of Nitrogen Fixation and Photosynthesis in Marine <italic toggle="yes">Trichodesmium</italic>10.1128/mSystems.00210-192379-5077https://doaj.org/article/02cc2bf524b947f98db48b55c0b6e8da2019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00210-19https://doaj.org/toc/2379-5077ABSTRACT The cyanobacterium Trichodesmium is an important contributor of new nitrogen (N) to the surface ocean, but its strategies for protecting the nitrogenase enzyme from inhibition by oxygen (O2) remain poorly understood. We present a dynamic physiological model to evaluate hypothesized conditions that would allow Trichodesmium to carry out its two conflicting metabolic processes of N2 fixation and photosynthesis. First, the model indicates that managing cellular O2 to permit N2 fixation requires high rates of respiratory O2 consumption. The energetic cost amounts to ∼80% of daily C fixation, comparable to the observed diminution of the growth rate of Trichodesmium relative to other phytoplankton. Second, by forming a trichome of connected cells, Trichodesmium can segregate N2 fixation from photosynthesis. The transfer of stored C to N-fixing cells fuels the respiratory O2 consumption that protects nitrogenase, while the reciprocal transfer of newly fixed N to C-fixing cells supports cellular growth. Third, despite Trichodesmium lacking the structural barrier found in heterocystous species, the model predicts low diffusivity of cell membranes, a function that may be explained by the presence of Gram-negative membrane, production of extracellular polysaccharide substances (EPS), and “buffer cells” that intervene between N2-fixing and photosynthetic cells. Our results suggest that all three factors—respiratory protection, trichome formation, and diffusion barriers—represent essential strategies that, despite their energetic costs, facilitate the growth of Trichodesmium in the oligotrophic aerobic ocean and permit it to be a major source of new reactive nitrogen. IMPORTANCE Trichodesmium is a major nitrogen-fixing cyanobacterium and exerts a significant influence on the oceanic nitrogen cycle. It is also a widely used model organism in laboratory studies. Since the nitrogen-fixing enzyme nitrogenase is extremely sensitive to oxygen, how these surface-dwelling plankton manage the two conflicting processes of nitrogen fixation and photosynthesis has been a long-standing question. In this study, we developed a simple model of metabolic fluxes of Trichodesmium capturing observed daily cycles of photosynthesis, nitrogen fixation, and boundary layer oxygen concentrations. The model suggests that forming a chain of cells for spatially segregating nitrogen fixation and photosynthesis is essential but not sufficient. It also requires a barrier against oxygen diffusion and high rates of oxygen scavenging by respiration. Finally, the model indicates that the life span of intracellular oxygen is extremely short, thus enabling cells to instantly create a low-oxygen environment upon deactivation of photosynthesis.Keisuke InomuraSamuel T. WilsonCurtis DeutschAmerican Society for MicrobiologyarticleTrichodesmiumcarbonnitrogennitrogen fixationnitrogenaseoxygenMicrobiologyQR1-502ENmSystems, Vol 4, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Trichodesmium carbon nitrogen nitrogen fixation nitrogenase oxygen Microbiology QR1-502
spellingShingle	Trichodesmium carbon nitrogen nitrogen fixation nitrogenase oxygen Microbiology QR1-502 Keisuke Inomura Samuel T. Wilson Curtis Deutsch Mechanistic Model for the Coexistence of Nitrogen Fixation and Photosynthesis in Marine <italic toggle="yes">Trichodesmium</italic>
description	ABSTRACT The cyanobacterium Trichodesmium is an important contributor of new nitrogen (N) to the surface ocean, but its strategies for protecting the nitrogenase enzyme from inhibition by oxygen (O2) remain poorly understood. We present a dynamic physiological model to evaluate hypothesized conditions that would allow Trichodesmium to carry out its two conflicting metabolic processes of N2 fixation and photosynthesis. First, the model indicates that managing cellular O2 to permit N2 fixation requires high rates of respiratory O2 consumption. The energetic cost amounts to ∼80% of daily C fixation, comparable to the observed diminution of the growth rate of Trichodesmium relative to other phytoplankton. Second, by forming a trichome of connected cells, Trichodesmium can segregate N2 fixation from photosynthesis. The transfer of stored C to N-fixing cells fuels the respiratory O2 consumption that protects nitrogenase, while the reciprocal transfer of newly fixed N to C-fixing cells supports cellular growth. Third, despite Trichodesmium lacking the structural barrier found in heterocystous species, the model predicts low diffusivity of cell membranes, a function that may be explained by the presence of Gram-negative membrane, production of extracellular polysaccharide substances (EPS), and “buffer cells” that intervene between N2-fixing and photosynthetic cells. Our results suggest that all three factors—respiratory protection, trichome formation, and diffusion barriers—represent essential strategies that, despite their energetic costs, facilitate the growth of Trichodesmium in the oligotrophic aerobic ocean and permit it to be a major source of new reactive nitrogen. IMPORTANCE Trichodesmium is a major nitrogen-fixing cyanobacterium and exerts a significant influence on the oceanic nitrogen cycle. It is also a widely used model organism in laboratory studies. Since the nitrogen-fixing enzyme nitrogenase is extremely sensitive to oxygen, how these surface-dwelling plankton manage the two conflicting processes of nitrogen fixation and photosynthesis has been a long-standing question. In this study, we developed a simple model of metabolic fluxes of Trichodesmium capturing observed daily cycles of photosynthesis, nitrogen fixation, and boundary layer oxygen concentrations. The model suggests that forming a chain of cells for spatially segregating nitrogen fixation and photosynthesis is essential but not sufficient. It also requires a barrier against oxygen diffusion and high rates of oxygen scavenging by respiration. Finally, the model indicates that the life span of intracellular oxygen is extremely short, thus enabling cells to instantly create a low-oxygen environment upon deactivation of photosynthesis.
format	article
author	Keisuke Inomura Samuel T. Wilson Curtis Deutsch
author_facet	Keisuke Inomura Samuel T. Wilson Curtis Deutsch
author_sort	Keisuke Inomura
title	Mechanistic Model for the Coexistence of Nitrogen Fixation and Photosynthesis in Marine <italic toggle="yes">Trichodesmium</italic>
title_short	Mechanistic Model for the Coexistence of Nitrogen Fixation and Photosynthesis in Marine <italic toggle="yes">Trichodesmium</italic>
title_full	Mechanistic Model for the Coexistence of Nitrogen Fixation and Photosynthesis in Marine <italic toggle="yes">Trichodesmium</italic>
title_fullStr	Mechanistic Model for the Coexistence of Nitrogen Fixation and Photosynthesis in Marine <italic toggle="yes">Trichodesmium</italic>
title_full_unstemmed	Mechanistic Model for the Coexistence of Nitrogen Fixation and Photosynthesis in Marine <italic toggle="yes">Trichodesmium</italic>
title_sort	mechanistic model for the coexistence of nitrogen fixation and photosynthesis in marine <italic toggle="yes">trichodesmium</italic>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/02cc2bf524b947f98db48b55c0b6e8da
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Mechanistic Model for the Coexistence of Nitrogen Fixation and Photosynthesis in Marine <italic toggle="yes">Trichodesmium</italic>

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