The tropical coral Pocillopora acuta displays an unusual chromatin structure and shows histone H3 clipping plasticity upon bleaching

Abstract

Background: Pocillopora acuta is a hermatypic coral with strong ecological importance. Anthropogenic disturbances and global warming are major threats that can induce coral bleaching, the disruption of the mutualistic symbiosis between the coral host and its endosymbiotic algae. Previous works have shown that somaclonal colonies display different levels of survival depending on the environmental conditions they previously faced. Epigenetic mechanisms are good candidates to explain this phenomenon. However, almost no work had been published on the P. acuta epigenome, especially on histone modifications. In this study, we aim at providing the first insight into chromatin structure of this species. Methods: We aligned the amino acid sequence of P. acuta core histones with histone sequences from various phyla. We developed a centri-filtration on sucrose gradient to separate chromatin from the host and the symbiont. The presence of histone H3 protein and specific histone modifications were then detected by western blot performed on histone extraction done from bleached and healthy corals. Finally, micrococcal nuclease (MNase) digestions were undertaken to study nucleosomal organization. Results: The centri-filtration enabled coral chromatin isolation with less than 2% of contamination by endosymbiont material. Histone sequences alignments with other species show that P. acuta displays on average ~90% of sequence similarities with mice and ~96% with other corals. H3 detection by western blot showed that H3 is clipped in healthy corals while it appeared to be intact in bleached corals. MNase treatment failed to provide the usual mononucleosomal digestion, a feature shared with some cnidarian, but not all; suggesting an unusual chromatin structure. Conclusions: These results provide a first insight into the chromatin, nucleosome and histone structure of P. acuta. The unusual patterns highlighted in this study and partly shared with other cnidarian will need to be further studied to better understand its role in corals.

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

“…Interestingly, histone acetylase and deacetylase activity have been shown to be influenced by microbes and dietary factors [10,42,43]. Although epigenetic studies in cnidarians remain scarce, there is evidence that histone modifications may play a critical role in host-algae symbiosis mechanisms [6,[44][45][46]. Here, we report the first genomic landscape of five histone modifications, H3K27me3, H3K36me3, H3K4me3, H3K27ac, and H3K9ac, in a symbiotic cnidarian.…”

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

“…Interestingly, histone acetylase and deacetylase activity have been shown to be influenced by microbes and dietary factors 15, 41, 42 . Although epigenetic studies in cnidarians remain scarce, there is evidence that histone modifications may play a critical role in host-algae symbiosis mechanisms 6, 43, 74, 75 . Here, we report the first genomic landscape of five histone modifications, H3K27me3, H3K36me3, H3K4me3, H3K27ac and H3K9ac, in a symbiotic cnidarian.…”

Epigenetics and Acquired Tolerance to Environmental Stress

“…Current studies employing nucleotide resolution of epigenetic marks in corals are limited to the study of DNA methylation. The studies on histone modifications available to date have instead used bulk assays based on enzyme-linked immunosorbent assays and western blotting to determine overall changes for the two histones H2A.X (Rodriguez-Casariego et al 2018) and H3 (Roquis et al 2021). These studies, however, showed that both histone variants respond to environmental changes.…”

“…These studies, however, showed that both histone variants respond to environmental changes. Western blot analysis of histone H3 in the coral Pocillopora acuta, for example, revealed unusual clipping in healthy colonies that was not present in bleached colonies (Roquis et al 2021). Histone clipping has been observed in a broad range of organisms from yeast to mammals and has been proposed to be involved in the regulation of various processes (Azad et al 2018).…”