Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia

Abstract

Background The symbiotic relationship between cnidarians and dinoflagellates is one of the most widespread endosymbiosis in our oceans and provides the ecological basis of coral reef ecosystems. Although many studies have been undertaken to unravel the molecular mechanisms underlying these symbioses, we still know little about the epigenetic mechanisms that control the transcriptional responses to symbiosis. Results Here, we used the model organism Exaiptasia diaphana to study the genome-wide patterns and putative functions of the histone modifications H3K27ac, H3K4me3, H3K9ac, H3K36me3, and H3K27me3 in symbiosis. While we find that their functions are generally conserved, we observed that colocalization of more than one modification and or DNA methylation correlated with significantly higher gene expression, suggesting a cooperative action of histone modifications and DNA methylation in promoting gene expression. Analysis of symbiosis genes revealed that activating histone modifications predominantly associated with symbiosis-induced genes involved in glucose metabolism, nitrogen transport, amino acid biosynthesis, and organism growth while symbiosis-suppressed genes were involved in catabolic processes. Conclusions Our results provide new insights into the mechanisms of prominent histone modifications and their interaction with DNA methylation in regulating symbiosis in cnidarians.

Unlocking the Complex Cell Biology of Coral–Dinoflagellate Symbiosis: A Model Systems Approach

“…Furthermore, proteomic studies comparing symbiotic with aposymbiotic Aiptasia, as well as symbiotic Aiptasia containing homologous versus heterologous symbionts, have also revealed important nutrient exchange mechanisms, including lipid and sterol transport by Niemann-Pick type C2 (NPC2) protein, inorganic carbon transport, and nitrogen cycling by members of the glutamine synthetase/glutamine oxoglutarate aminotransferase (GS/GOGAT) pathway (111,143). In Aiptasia hosting a homologous symbiont strain, a deep analysis into host gene regulation demonstrated that the activation of histone modifications was associated with genes upregulated in symbiosis, including glucose metabolism, nitrogen transport, and members of mTORC1, among others (107). At the cellular level, single-cell RNA sequencing of the stony coral S. pistillata demonstrated that symbiont-containing cells upregulate lysosome-associated genes, as well as genes involved in lipid sensing and metabolism, from transport to fatty acid elongation (77).…”

Genome-wide profiling of histone (H3) lysine 4 (K4) tri-methylation (me3) under drought, heat, and combined stresses in switchgrass

“…This is compatible with recent findings in Arabidopsis that the H3K4me3 mark was significant in TSS and genic regions [ 60 , 65 , 68 , 69 ], indicating that domains might be conserved in organisms [ 45 , 70 , 71 ]. Species-specific H3K4me3 distribution patterns were reported in plants, while some genomes were highly methylated, and a few were sparsely methylated [ 72 – 74 ]. The epigenetic mechanisms often act in a coordinated fashion to influence plant functions.…”