Periodic and coordinated gene expression between a diazotroph and its diatom host

Abstract

In the surface ocean, light fuels photosynthetic carbon fixation of phytoplankton, playing a critical role in ecosystem processes including carbon export to the deep sea. In oligotrophic oceans, diatom-diazotroph associations (DDAs) play a keystone role in ecosystem function because diazotrophs can provide otherwise scarce biologically available nitrogen to the diatom host, fueling growth and subsequent carbon sequestration. Despite their importance, relatively little is known about the nature of these associations in situ. Here we used metatranscriptomic sequencing of surface samples from the North Pacific Subtropical Gyre (NPSG) to reconstruct patterns of gene expression for the diazotrophic symbiont Richelia and we examined how these patterns were integrated with those of the diatom host over day-night transitions. Richelia exhibited significant diel signals for genes related to photosynthesis, N fixation, and resource acquisition, among other processes. N fixation genes were significantly co-expressed with host nitrogen uptake and metabolism, as well as potential genes involved in carbon transport, which may underpin the exchange of nitrogen and carbon within this association. Patterns of expression suggested cell division was integrated between the host and symbiont across the diel cycle. Collectively these data suggest that symbiont-host physiological ecology is strongly interconnected in the NPSG.

A transcriptional cycle suited to daytime N2 fixation in the unicellular cyanobacterium Candidatus Atelocyanobacterium thalassa (UCYN-A)

“…High levels of phosphate transporters during the day could meet the increased demand for inorganic phosphate (33, 34) during DNA replication, which occurs during the day in UCYN-A and Trichosdesmium . Similar patterns were observed in the heterocyst-forming Richelia with peak expression of P acquisition genes at approximately 15:00, suggesting the apparent rhythmicity of P acquisition could be a common feature of daytime N 2 -fixers (35).…”

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

“…Based on the size differences, the diatom contains 4.5 times more N than the trichomes. Assuming that the diatom's N demand is fully covered by the N 2 -fixing symbiont [1,6] and that both organisms grow at the same speed (which is required if the symbiosis is in steady-state growth [51,52]), the model predicts that the trichome must fix N 2 5.5 times faster than in the hypothetical case without the host. This increase has been observed in analogous systems.…”

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

“…the Rhizosolenia host and symbiont DDA were tightly coupled (Harke et al 2019). There are at least two mechanisms that could produce this result in the Rhizosolenia DDA: downregulation of symbiont diazotrophy by exposure to NO 3due to its extra-plasmalemma location and/or induction of host nitrate reductase pathways.…”