Carbon transfer from the host diatom enables fast growth and high rate of N2 fixation by symbiotic heterocystous cyanobacteria

Diatom–diazotroph associations (DDAs) are symbioses where trichome-forming cyanobacteria support the host diatom with fixed nitrogen through dinitrogen (N2) fixation. It is inferred that the growth of the trichomes is also supported by the host, but the support mechanism has not been fully quantifie...

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Main Authors: Inomura, Keisuke, Follett, Christopher L, Masuda, Takako, Eichner, Meri, Prášil, Ondřej, Deutsch, Curtis
Other Authors: Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences
Format: Article
Published: Multidisciplinary Digital Publishing Institute 2020
Online Access:https://hdl.handle.net/1721.1/125560
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author Inomura, Keisuke
Follett, Christopher L
Masuda, Takako
Eichner, Meri
Prášil, Ondřej
Deutsch, Curtis
author2 Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences
author_facet Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences
Inomura, Keisuke
Follett, Christopher L
Masuda, Takako
Eichner, Meri
Prášil, Ondřej
Deutsch, Curtis
author_sort Inomura, Keisuke
collection MIT
description Diatom–diazotroph associations (DDAs) are symbioses where trichome-forming cyanobacteria support the host diatom with fixed nitrogen through dinitrogen (N2) 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 N2 fixation rate by the trichomes. The model predicts that the rate of N2 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 N2 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 N2 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 N2 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 N2 fixation in symbiotic trichomes relative to other aquatic diazotrophs. Keywords: DDA; nitrogen fixation; diatom; diazotroph; carbon; nitrogen; growth rate; photosynthesis; cell flux model
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spelling mit-1721.1/1255602022-09-29T10:06:44Z Carbon transfer from the host diatom enables fast growth and high rate of N2 fixation by symbiotic heterocystous cyanobacteria Carbon transfer from the host diatom enables fast growth and high rate of N[subscript 2] fixation by symbiotic heterocystous cyanobacteria Inomura, Keisuke Follett, Christopher L Masuda, Takako Eichner, Meri Prášil, Ondřej Deutsch, Curtis Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences Diatom–diazotroph associations (DDAs) are symbioses where trichome-forming cyanobacteria support the host diatom with fixed nitrogen through dinitrogen (N2) 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 N2 fixation rate by the trichomes. The model predicts that the rate of N2 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 N2 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 N2 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 N2 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 N2 fixation in symbiotic trichomes relative to other aquatic diazotrophs. Keywords: DDA; nitrogen fixation; diatom; diazotroph; carbon; nitrogen; growth rate; photosynthesis; cell flux model Simons CBIOMES Postdoctoral Fellowship (award no. 553242) 2020-05-28T17:28:17Z 2020-05-28T17:28:17Z 2020-02-04 2019-12 2020-03-02T13:02:16Z Article http://purl.org/eprint/type/JournalArticle 2223-7747 https://hdl.handle.net/1721.1/125560 Inomura, Keisuke, et al., "Carbon transfer from the host diatom enables fast growth and high rate of N2 fixation by symbiotic heterocystous cyanobacteria." Plants 9, 2 (2020): no. 192 doi 10.3390/plants9020192 ©2020 Author(s) 10.3390/plants9020192 Plants Creative Commons Attribution https://creativecommons.org/licenses/by/4.0/ application/pdf Multidisciplinary Digital Publishing Institute Multidisciplinary Digital Publishing Institute
spellingShingle 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 N2 fixation by symbiotic heterocystous cyanobacteria
title Carbon transfer from the host diatom enables fast growth and high rate of N2 fixation by symbiotic heterocystous cyanobacteria
title_full Carbon transfer from the host diatom enables fast growth and high rate of N2 fixation by symbiotic heterocystous cyanobacteria
title_fullStr Carbon transfer from the host diatom enables fast growth and high rate of N2 fixation by symbiotic heterocystous cyanobacteria
title_full_unstemmed Carbon transfer from the host diatom enables fast growth and high rate of N2 fixation by symbiotic heterocystous cyanobacteria
title_short Carbon transfer from the host diatom enables fast growth and high rate of N2 fixation by symbiotic heterocystous cyanobacteria
title_sort carbon transfer from the host diatom enables fast growth and high rate of n2 fixation by symbiotic heterocystous cyanobacteria
url https://hdl.handle.net/1721.1/125560
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