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...

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Main Authors: Kashif Nawaz, Maha J. Cziesielski, Kiruthiga G. Mariappan, Guoxin Cui, Manuel Aranda
Format: Article
Language:English
Published: BMC 2022-12-01
Series:BMC Biology
Subjects:
Online Access:https://doi.org/10.1186/s12915-022-01469-y
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author Kashif Nawaz
Maha J. Cziesielski
Kiruthiga G. Mariappan
Guoxin Cui
Manuel Aranda
author_facet Kashif Nawaz
Maha J. Cziesielski
Kiruthiga G. Mariappan
Guoxin Cui
Manuel Aranda
author_sort Kashif Nawaz
collection DOAJ
description 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.
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spelling doaj.art-802f899c277e438abcba53b400ad1e4b2022-12-22T04:17:29ZengBMCBMC Biology1741-70072022-12-0120111710.1186/s12915-022-01469-yHistone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone AiptasiaKashif Nawaz0Maha J. Cziesielski1Kiruthiga G. Mariappan2Guoxin Cui3Manuel Aranda4Marine Science Program, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology (KAUST)Marine Science Program, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology (KAUST)Marine Science Program, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology (KAUST)Marine Science Program, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology (KAUST)Marine Science Program, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology (KAUST)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.https://doi.org/10.1186/s12915-022-01469-ySymbiosisCoralsClimate ChangeEpigeneticsHistone modifications
spellingShingle Kashif Nawaz
Maha J. Cziesielski
Kiruthiga G. Mariappan
Guoxin Cui
Manuel Aranda
Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia
BMC Biology
Symbiosis
Corals
Climate Change
Epigenetics
Histone modifications
title Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia
title_full Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia
title_fullStr Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia
title_full_unstemmed Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia
title_short Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia
title_sort histone modifications and dna methylation act cooperatively in regulating symbiosis genes in the sea anemone aiptasia
topic Symbiosis
Corals
Climate Change
Epigenetics
Histone modifications
url https://doi.org/10.1186/s12915-022-01469-y
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