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

Abstract

ABSTRACTMany 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 coralOculina arbusculaby 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.