DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral model Aiptasia

Yong Li; Yi Jin Liew; Guoxin Cui; Maha Joana Cziesielski; Noura Ibrahim Omar Zahran; Craig Michell; Christian R. Voolstra; Manuel Aranda

doi:10.1126/sciadv.aat2142

DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral model Aiptasia

Yong Li, Yi Jin Liew, Guoxin Cui, Maha Joana Cziesielski, Noura Ibrahim Omar Zahran, Craig Michell, Christian R. Voolstra, Manuel Aranda

Research output: Contribution to journal › Article › peer-review

22 Scopus citations

Abstract

The symbiotic relationship between cnidarians and dinoflagellates is the cornerstone of coral reef ecosystems. Although research has focused on the molecular mechanisms underlying this symbiosis, the role of epigenetic mechanisms, that is, the study of heritable changes that do not involve changes in the DNA sequence, is unknown. To assess the role of DNA methylation in the cnidarian-dinoflagellate symbiosis, we analyzed genome-wide CpG methylation, histone associations, and transcriptomic states of symbiotic and aposymbiotic anemones in the model system Aiptasia. We found that methylated genes are marked by histone 3 lysine 36 trimethylation (H3K36me3) and show significant reduction of spurious transcription and transcriptional noise, revealing a role of DNA methylation in the maintenance of transcriptional homeostasis. Changes in DNA methylation and expression show enrichment for symbiosis-related processes, such as immunity, apoptosis, phagocytosis recognition, and phagosome formation, and reveal intricate interactions between the underlying pathways. Our results demonstrate that DNA methylation provides an epigenetic mechanism of transcriptional homeostasis that responds to symbiosis.

Original language	English (US)
Pages (from-to)	eaat2142
Journal	Science Advances
Volume	4
Issue number	8
DOIs	https://doi.org/10.1126/sciadv.aat2142
State	Published - Aug 15 2018

Access to Document

10.1126/sciadv.aat2142

https://repository.kaust.edu.sa/bitstream/10754/628481/1/eaat2142.full.pdf

Fingerprint Dive into the research topics of 'DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral model Aiptasia'. Together they form a unique fingerprint.

Aiptasia whole-genome bisulfite sequencing (DNA methylation) on cnidarian-dinoflagellate symbiosis
Cui, G. (Creator), Liew, Y. J. (Creator), Li, Y. (Creator), Kharbatia, N. M. (Creator), Zahran, N. I. O. (Creator), Emwas, A. M. (Creator), Eguiluz, V. M. (Creator), Aranda, M. (Creator) & Eguiluz, V. M. (Creator), NCBI, Oct 23 2017
http://hdl.handle.net/10754/666486
Dataset

Cite this

@article{9bfcc9ac690d43079efa42adac8e080a,

title = "DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral model Aiptasia",

abstract = "The symbiotic relationship between cnidarians and dinoflagellates is the cornerstone of coral reef ecosystems. Although research has focused on the molecular mechanisms underlying this symbiosis, the role of epigenetic mechanisms, that is, the study of heritable changes that do not involve changes in the DNA sequence, is unknown. To assess the role of DNA methylation in the cnidarian-dinoflagellate symbiosis, we analyzed genome-wide CpG methylation, histone associations, and transcriptomic states of symbiotic and aposymbiotic anemones in the model system Aiptasia. We found that methylated genes are marked by histone 3 lysine 36 trimethylation (H3K36me3) and show significant reduction of spurious transcription and transcriptional noise, revealing a role of DNA methylation in the maintenance of transcriptional homeostasis. Changes in DNA methylation and expression show enrichment for symbiosis-related processes, such as immunity, apoptosis, phagocytosis recognition, and phagosome formation, and reveal intricate interactions between the underlying pathways. Our results demonstrate that DNA methylation provides an epigenetic mechanism of transcriptional homeostasis that responds to symbiosis.",

author = "Yong Li and Liew, {Yi Jin} and Guoxin Cui and Cziesielski, {Maha Joana} and Zahran, {Noura Ibrahim Omar} and Craig Michell and Voolstra, {Christian R.} and Manuel Aranda",

note = "KAUST Repository Item: Exported on 2021-02-19 Acknowledgements: Acknowledgments: We thank J. Pringle for the provision of the initial Aiptasia CC7 and Symbiodinium SSB01 cultures. We thank S. Baumgarten for his help with establishing the Aiptasia cultures and critical reading of the manuscript. We also thank the four anonymous reviewers for their effort and valuable suggestions, which greatly improved this study. Funding: Research reported in this publication was supported by baseline funding from the King Abdullah University of Science and Technology to M.A.",

year = "2018",

month = aug,

day = "15",

doi = "10.1126/sciadv.aat2142",

language = "English (US)",

volume = "4",

pages = "eaat2142",

journal = "Science Advances",

issn = "2375-2548",

publisher = "American Association for the Advancement of Science",

number = "8",

}

DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral model Aiptasia. / Li, Yong; Liew, Yi Jin; Cui, Guoxin; Cziesielski, Maha Joana; Zahran, Noura Ibrahim Omar; Michell, Craig; Voolstra, Christian R.; Aranda, Manuel.

In: Science Advances, Vol. 4, No. 8, 15.08.2018, p. eaat2142.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral model Aiptasia

AU - Li, Yong

AU - Liew, Yi Jin

AU - Cui, Guoxin

AU - Cziesielski, Maha Joana

AU - Zahran, Noura Ibrahim Omar

AU - Michell, Craig

AU - Voolstra, Christian R.

AU - Aranda, Manuel

N1 - KAUST Repository Item: Exported on 2021-02-19 Acknowledgements: Acknowledgments: We thank J. Pringle for the provision of the initial Aiptasia CC7 and Symbiodinium SSB01 cultures. We thank S. Baumgarten for his help with establishing the Aiptasia cultures and critical reading of the manuscript. We also thank the four anonymous reviewers for their effort and valuable suggestions, which greatly improved this study. Funding: Research reported in this publication was supported by baseline funding from the King Abdullah University of Science and Technology to M.A.

PY - 2018/8/15

Y1 - 2018/8/15

N2 - The symbiotic relationship between cnidarians and dinoflagellates is the cornerstone of coral reef ecosystems. Although research has focused on the molecular mechanisms underlying this symbiosis, the role of epigenetic mechanisms, that is, the study of heritable changes that do not involve changes in the DNA sequence, is unknown. To assess the role of DNA methylation in the cnidarian-dinoflagellate symbiosis, we analyzed genome-wide CpG methylation, histone associations, and transcriptomic states of symbiotic and aposymbiotic anemones in the model system Aiptasia. We found that methylated genes are marked by histone 3 lysine 36 trimethylation (H3K36me3) and show significant reduction of spurious transcription and transcriptional noise, revealing a role of DNA methylation in the maintenance of transcriptional homeostasis. Changes in DNA methylation and expression show enrichment for symbiosis-related processes, such as immunity, apoptosis, phagocytosis recognition, and phagosome formation, and reveal intricate interactions between the underlying pathways. Our results demonstrate that DNA methylation provides an epigenetic mechanism of transcriptional homeostasis that responds to symbiosis.

AB - The symbiotic relationship between cnidarians and dinoflagellates is the cornerstone of coral reef ecosystems. Although research has focused on the molecular mechanisms underlying this symbiosis, the role of epigenetic mechanisms, that is, the study of heritable changes that do not involve changes in the DNA sequence, is unknown. To assess the role of DNA methylation in the cnidarian-dinoflagellate symbiosis, we analyzed genome-wide CpG methylation, histone associations, and transcriptomic states of symbiotic and aposymbiotic anemones in the model system Aiptasia. We found that methylated genes are marked by histone 3 lysine 36 trimethylation (H3K36me3) and show significant reduction of spurious transcription and transcriptional noise, revealing a role of DNA methylation in the maintenance of transcriptional homeostasis. Changes in DNA methylation and expression show enrichment for symbiosis-related processes, such as immunity, apoptosis, phagocytosis recognition, and phagosome formation, and reveal intricate interactions between the underlying pathways. Our results demonstrate that DNA methylation provides an epigenetic mechanism of transcriptional homeostasis that responds to symbiosis.

UR - http://hdl.handle.net/10754/628481

UR - http://advances.sciencemag.org/content/4/8/eaat2142

UR - http://www.scopus.com/inward/record.url?scp=85052202995&partnerID=8YFLogxK

U2 - 10.1126/sciadv.aat2142

DO - 10.1126/sciadv.aat2142

M3 - Article

C2 - 30116782

AN - SCOPUS:85052202995

VL - 4

SP - eaat2142

JO - Science Advances

JF - Science Advances

SN - 2375-2548

IS - 8

ER -

DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral model Aiptasia

Abstract

Access to Document

Other files and links

Aiptasia whole-genome bisulfite sequencing (DNA methylation) on cnidarian-dinoflagellate symbiosis

Cite this