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Carbon Transfer from the Host Diatom Enables Fast Growth and High Rate of N(2) Fixation by Symbiotic Heterocystous Cyanobacteria

Diatom–diazotroph associations (DDAs) are symbioses where trichome-forming cyanobacteria support the host diatom with fixed nitrogen through dinitrogen (N(2)) fixation. It is inferred that the growth of the trichomes is also supported by the host, but the support mechanism has not been fully quantif...

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Autores principales: Inomura, Keisuke, Follett, Christopher L., Masuda, Takako, Eichner, Meri, Prášil, Ondřej, Deutsch, Curtis
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7076409/
https://www.ncbi.nlm.nih.gov/pubmed/32033207
http://dx.doi.org/10.3390/plants9020192
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author Inomura, Keisuke
Follett, Christopher L.
Masuda, Takako
Eichner, Meri
Prášil, Ondřej
Deutsch, Curtis
author_facet Inomura, Keisuke
Follett, Christopher L.
Masuda, Takako
Eichner, Meri
Prášil, Ondřej
Deutsch, Curtis
author_sort Inomura, Keisuke
collection PubMed
description Diatom–diazotroph associations (DDAs) are symbioses where trichome-forming cyanobacteria support the host diatom with fixed nitrogen through dinitrogen (N(2)) fixation. It is inferred that the growth of the trichomes is also supported by the host, but the support mechanism has not been fully quantified. Here, we develop a coarse-grained, cellular model of the symbiosis between Hemiaulus and Richelia (one of the major DDAs), which shows that carbon (C) transfer from the diatom enables a faster growth and N(2) fixation rate by the trichomes. The model predicts that the rate of N(2) fixation is 5.5 times that of the hypothetical case without nitrogen (N) transfer to the host diatom. The model estimates that 25% of fixed C from the host diatom is transferred to the symbiotic trichomes to support the high rate of N(2) fixation. In turn, 82% of N fixed by the trichomes ends up in the host. Modeled C fixation from the vegetative cells in the trichomes supports only one-third of their total C needs. Even if we ignore the C cost for N(2) fixation and for N transfer to the host, the total C cost of the trichomes is higher than the C supply by their own photosynthesis. Having more trichomes in a single host diatom decreases the demand for N(2) fixation per trichome and thus decreases their cost of C. However, even with five trichomes, which is about the highest observed for Hemiaulus and Richelia symbiosis, the model still predicts a significant C transfer from the diatom host. These results help quantitatively explain the observed high rates of growth and N(2) fixation in symbiotic trichomes relative to other aquatic diazotrophs.
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spelling pubmed-70764092020-03-24 Carbon Transfer from the Host Diatom Enables Fast Growth and High Rate of N(2) Fixation by Symbiotic Heterocystous Cyanobacteria Inomura, Keisuke Follett, Christopher L. Masuda, Takako Eichner, Meri Prášil, Ondřej Deutsch, Curtis Plants (Basel) Article Diatom–diazotroph associations (DDAs) are symbioses where trichome-forming cyanobacteria support the host diatom with fixed nitrogen through dinitrogen (N(2)) fixation. It is inferred that the growth of the trichomes is also supported by the host, but the support mechanism has not been fully quantified. Here, we develop a coarse-grained, cellular model of the symbiosis between Hemiaulus and Richelia (one of the major DDAs), which shows that carbon (C) transfer from the diatom enables a faster growth and N(2) fixation rate by the trichomes. The model predicts that the rate of N(2) fixation is 5.5 times that of the hypothetical case without nitrogen (N) transfer to the host diatom. The model estimates that 25% of fixed C from the host diatom is transferred to the symbiotic trichomes to support the high rate of N(2) fixation. In turn, 82% of N fixed by the trichomes ends up in the host. Modeled C fixation from the vegetative cells in the trichomes supports only one-third of their total C needs. Even if we ignore the C cost for N(2) fixation and for N transfer to the host, the total C cost of the trichomes is higher than the C supply by their own photosynthesis. Having more trichomes in a single host diatom decreases the demand for N(2) fixation per trichome and thus decreases their cost of C. However, even with five trichomes, which is about the highest observed for Hemiaulus and Richelia symbiosis, the model still predicts a significant C transfer from the diatom host. These results help quantitatively explain the observed high rates of growth and N(2) fixation in symbiotic trichomes relative to other aquatic diazotrophs. MDPI 2020-02-04 /pmc/articles/PMC7076409/ /pubmed/32033207 http://dx.doi.org/10.3390/plants9020192 Text en © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Inomura, Keisuke
Follett, Christopher L.
Masuda, Takako
Eichner, Meri
Prášil, Ondřej
Deutsch, Curtis
Carbon Transfer from the Host Diatom Enables Fast Growth and High Rate of N(2) Fixation by Symbiotic Heterocystous Cyanobacteria
title Carbon Transfer from the Host Diatom Enables Fast Growth and High Rate of N(2) Fixation by Symbiotic Heterocystous Cyanobacteria
title_full Carbon Transfer from the Host Diatom Enables Fast Growth and High Rate of N(2) Fixation by Symbiotic Heterocystous Cyanobacteria
title_fullStr Carbon Transfer from the Host Diatom Enables Fast Growth and High Rate of N(2) Fixation by Symbiotic Heterocystous Cyanobacteria
title_full_unstemmed Carbon Transfer from the Host Diatom Enables Fast Growth and High Rate of N(2) Fixation by Symbiotic Heterocystous Cyanobacteria
title_short Carbon Transfer from the Host Diatom Enables Fast Growth and High Rate of N(2) Fixation by Symbiotic Heterocystous Cyanobacteria
title_sort carbon transfer from the host diatom enables fast growth and high rate of n(2) fixation by symbiotic heterocystous cyanobacteria
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7076409/
https://www.ncbi.nlm.nih.gov/pubmed/32033207
http://dx.doi.org/10.3390/plants9020192
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