Carbon Transfer from the Host Diatom Enables Fast Growth and High Rate of N2 Fixation by Symbiotic Heterocystous Cyanobacteria

Abstract

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.

Isolation, growth, and nitrogen fixation rates of the Hemiaulus-Richelia (diatom-cyanobacterium) symbiosis in culture

“…Our report presents the full range of data in Pyle's work and notes that rates can be~0.2 div d −1 higher than the values used by Follett et al (2018) depending on the strain used. These higher rates are consistent with the mechanistic model of Inomura et al (2020) in that host carbon fixation is substantial enough support to the symbiont N 2 fixation rates required for the unit DDA growth. This host derived carbon is likely to also be the reductant and energy source required to support the lengthy decline of N 2 fixation rates at the beginning of the scotophase noted in the diel experiment (Fig.…”

“…(no information on symbionts) has been reported with growth rates up to 2.2 div d −1 ( Furnas, 1991 ) in field experiments and 3.8 div d −1 in nitrate-based laboratory medium ( Brand & Guillard, 1981 ). While the symbiont presence is undocumented but seems unlikely given the DDA growth rates reported in our paper of <1.0 div d −1 as well as by modeled symbiont diazotrophy ( Inomura et al, 2020 ). The Furnas (1991) and Brand & Guillard (1981) reports, as well as our briefly established asymbiotic strain on medium that would not support Hemiaulus DDA growth, all suggest that symbiont-free strains of Hemiaulus are extant in the modern ocean.…”

“…However, damaging effects by solar UV wavelengths (Zhu et al, 2020) require further examination. Follett et al (2018) and Inomura et al (2020) utilized H. hauckii DDA growth rates extracted from Pyle (2011) for modeling applications. Our report presents the full range of data in Pyle's work and notes that rates can be~0.2 div d −1 higher than the values used by Follett et al (2018) depending on the strain used.…”

Peer Review #2 of "Isolation, growth, and nitrogen fixation rates of the Hemiaulus-Richelia (diatom-cyanobacterium) symbiosis in culture (v0.2)"

“…(2018) depending on the strain used. These higher rates are consistent with the mechanistic model of Inomura et al (2020) in that host carbon fixation is substantial enough support to the symbiont N 2 fixation rates required for the unit DDA growth. This host derived carbon is likely to also be the reductant and energy source required to support the lengthy decline of N 2 fixation rates at the beginning of the scotophase noted in the diel experiment (Fig.…”

Peer Review #1 of "Isolation, growth, and nitrogen fixation rates of the Hemiaulus-Richelia (diatom-cyanobacterium) symbiosis in culture (v0.1)"

“…(no information on symbionts) has been reported with growth rates up to 2.2 div d -1 (Furnas 1991) in field experiments and 3.8 div d -1 in nitrate-based laboratory medium (Brand & Guillard 1981). While the symbiont presence is undocumented but seems unlikely given the DDA growth rates reported in our paper of <1.0 div d -1 as well as by modelled symbiont diazotrophy (Inomura et al 2020). The Furnas (1991) and Brand & Guillard (1981) Manuscript to be reviewed growth rates > 1 div d -1 with asymbiotic cells growing on ambient N at somewhat greater rates.…”