Quantifying Oxygen Management and Temperature and Light Dependencies of Nitrogen Fixation by <named-content content-type="genus-species">Crocosphaera watsonii</named-content>

ABSTRACT 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 d...

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Autores principales:	Keisuke Inomura, Curtis Deutsch, Samuel T. Wilson, Takako Masuda, Evelyn Lawrenz, Lenka Bučinská, Roman Sobotka, Julia M. Gauglitz, Mak A. Saito, Ondřej Prášil, Michael J. Follows
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Crocosphaera carbon cell flux model daily cycle iron light Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f846d31ec90341dd8104af1cc09b94ff
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spelling	oai:doaj.org-article:f846d31ec90341dd8104af1cc09b94ff2021-11-15T15:22:24ZQuantifying Oxygen Management and Temperature and Light Dependencies of Nitrogen Fixation by <named-content content-type="genus-species">Crocosphaera watsonii</named-content>10.1128/mSphere.00531-192379-5042https://doaj.org/article/f846d31ec90341dd8104af1cc09b94ff2019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00531-19https://doaj.org/toc/2379-5042ABSTRACT 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. IMPORTANCE Crocosphaera is one of the major N2-fixing microorganisms in the open ocean. On a global scale, the process of N2 fixation is important in balancing the N budget, but the factors governing the rate of N2 fixation remain poorly resolved. Here, we combine a mechanistic model and both previous and present laboratory studies of Crocosphaera to quantify how chemical factors such as C, N, Fe, and O2 and physical factors such as temperature and light affect N2 fixation. Our study shows that Crocosphaera combines multiple mechanisms to reduce intracellular O2 to protect the O2-sensitive N2-fixing enzyme. Our model, however, indicates that these protections are insufficient at low temperature due to reduced respiration and the rate of N2 fixation becomes severely limited. This provides a physiological explanation for why the geographic distribution of Crocosphaera is confined to the warm low-latitude ocean.Keisuke InomuraCurtis DeutschSamuel T. WilsonTakako MasudaEvelyn LawrenzLenka BučinskáRoman SobotkaJulia M. GauglitzMak A. SaitoOndřej PrášilMichael J. FollowsAmerican Society for MicrobiologyarticleCrocosphaeracarboncell flux modeldaily cycleironlightMicrobiologyQR1-502ENmSphere, Vol 4, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Crocosphaera carbon cell flux model daily cycle iron light Microbiology QR1-502
spellingShingle	Crocosphaera carbon cell flux model daily cycle iron light Microbiology QR1-502 Keisuke Inomura Curtis Deutsch Samuel T. Wilson Takako Masuda Evelyn Lawrenz Lenka Bučinská Roman Sobotka Julia M. Gauglitz Mak A. Saito Ondřej Prášil Michael J. Follows Quantifying Oxygen Management and Temperature and Light Dependencies of Nitrogen Fixation by <named-content content-type="genus-species">Crocosphaera watsonii</named-content>
description	ABSTRACT 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. IMPORTANCE Crocosphaera is one of the major N2-fixing microorganisms in the open ocean. On a global scale, the process of N2 fixation is important in balancing the N budget, but the factors governing the rate of N2 fixation remain poorly resolved. Here, we combine a mechanistic model and both previous and present laboratory studies of Crocosphaera to quantify how chemical factors such as C, N, Fe, and O2 and physical factors such as temperature and light affect N2 fixation. Our study shows that Crocosphaera combines multiple mechanisms to reduce intracellular O2 to protect the O2-sensitive N2-fixing enzyme. Our model, however, indicates that these protections are insufficient at low temperature due to reduced respiration and the rate of N2 fixation becomes severely limited. This provides a physiological explanation for why the geographic distribution of Crocosphaera is confined to the warm low-latitude ocean.
format	article
author	Keisuke Inomura Curtis Deutsch Samuel T. Wilson Takako Masuda Evelyn Lawrenz Lenka Bučinská Roman Sobotka Julia M. Gauglitz Mak A. Saito Ondřej Prášil Michael J. Follows
author_facet	Keisuke Inomura Curtis Deutsch Samuel T. Wilson Takako Masuda Evelyn Lawrenz Lenka Bučinská Roman Sobotka Julia M. Gauglitz Mak A. Saito Ondřej Prášil Michael J. Follows
author_sort	Keisuke Inomura
title	Quantifying Oxygen Management and Temperature and Light Dependencies of Nitrogen Fixation by <named-content content-type="genus-species">Crocosphaera watsonii</named-content>
title_short	Quantifying Oxygen Management and Temperature and Light Dependencies of Nitrogen Fixation by <named-content content-type="genus-species">Crocosphaera watsonii</named-content>
title_full	Quantifying Oxygen Management and Temperature and Light Dependencies of Nitrogen Fixation by <named-content content-type="genus-species">Crocosphaera watsonii</named-content>
title_fullStr	Quantifying Oxygen Management and Temperature and Light Dependencies of Nitrogen Fixation by <named-content content-type="genus-species">Crocosphaera watsonii</named-content>
title_full_unstemmed	Quantifying Oxygen Management and Temperature and Light Dependencies of Nitrogen Fixation by <named-content content-type="genus-species">Crocosphaera watsonii</named-content>
title_sort	quantifying oxygen management and temperature and light dependencies of nitrogen fixation by <named-content content-type="genus-species">crocosphaera watsonii</named-content>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/f846d31ec90341dd8104af1cc09b94ff
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Quantifying Oxygen Management and Temperature and Light Dependencies of Nitrogen Fixation by <named-content content-type="genus-species">Crocosphaera watsonii</named-content>

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