Single-cell RNA-sequencing reveals immune system compartmentalization under symbiosis in the stony coral Oculina arbuscula

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Abstract

Many cnidarians host single-celled algae within gastrodermal cells, yielding a mutually beneficial exchange of nutrients between host and symbiont, and dysbiosis can lead to host mortality. Previous research has uncovered symbiosis tradeoffs, including suppression of the NF-κB immune pathway in cnidarians hosting intracellular algae and correlations between symbiotic state and pathogen susceptibility. Here, we used a multiomic approach to characterize symbiotic states of the facultatively symbiotic coral Oculina arbuscula by generating genotype-controlled fragments of symbiotic and aposymbiotic tissue. Metabarcoding of 16S rRNA showed no difference in bacterial communities between symbiotic states. Consistent with previous whole-organism RNA-seq studies, whole-organism proteomics revealed differential abundance of proteins related to immunity, consistent with immune suppression during symbiosis. Moreover, single-cell RNAseq identified diverse cell clusters within six cell types across symbiotic states. Specifically, the gastrodermal cell cluster containing algal-hosting cells from symbiotic tissue had higher expression of nitrogen cycling and sugar transport genes than gastrodermal cells from aposymbiotic tissue. Furthermore, lower expression of genes involved in immune regulation, including NF-κB pathway genes, was observed in these gastrodermal cells from symbiotic tissue. However, no differences in gene expression in the immune cell cluster were observed between symbiotic states. This work reveals a compartmentalization of immune system suppression in specific gastrodermal cells in symbiosis, which likely limits symbiosis tradeoffs by dampening immunity in algal hosting cells while still maintaining general organismal immunity.

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  1. host immunity is modulated to facilitate endosymbiosis

    It would be useful to show a schematic of the differences in aposymbiotic and symbiotic stony corals, kind of like a graphical abstract. The abstract was hard to follow without reading the details of the study, and it would be nice to see the overall findings in a visual way. This could get across the idea that neither the bacterial communities nor the proportion of immune cells differ between symbiotic states, but the gastrodermis I cells downregulate immune genes when algae is in close contact. That begs the question, will you follow up to determine what chemical cues from the algae are sensed by the gastrodermis cells to alter their gene expression?

  2. aposymbiotic branches were transferred back to common garden aquaria and maintained for at least 2 months of recovery prior to physiological and multiomic profiling

    How do these corals acquire their symbionts? Is it surprising that with 2 months of recovery following the bleaching even that the symbiont load remained so low? Or is there a sensitive window that has closed for corals at this stage of development?