The methylome of Biomphalaria glabrata and other mollusks: enduring modification of epigenetic landscape and phenotypic traits by a new DNA methylation inhibitor

Type Article
Date 2021-10
Language English
Author(s) Luviano Nelia1, Lopez Marie2, 3, Gawehns Fleur4, Chaparro Cristian1, Arimondo Paola B.3, 5, Ivanovic Slavica6, David Patrice7, Verhoeven Koen6, Cosseau Céline1, Grunau ChristophORCID1
Affiliation(s) 1 : IHPE, Univ Perpignan Via Domitia, CNRC, Ifremer, Univ Montpellier, Perpignan, France
2 : Institut des Biomolécules Max Mousseron (IBMM), UMR 5247, CNRS, Univ Montpellier, ENSCM, Montpellier, France
3 : Epigenetic Targeting of Cancer (ETaC), CNRS FRE3600, Centre de Recherche et Développement Pierre Fabre, Toulouse, France
4 : Bioinformatics Unit, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands
5 : Epigenetic Chemical Biology (EpiChBio), Department Structural Biology and Chemistry, UMR 3523, CNRS, Institute Pasteur, 75015, Paris, France
6 : Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands
7 : Centre d’Ecologie Fonctionnelle et Evolutive (CEFE), Univ. Montpellier, CNRS - Université Paul Valéry Montpellier - EPHE, 1919 Route de Mende, 34293, Montpellier Cedex 5, France
Source Epigenetics & Chromatin (1756-8935) (Springer Science and Business Media LLC), 2021-10 , Vol. 14 , N. 1 , P. 48 (25p.)
DOI 10.1186/s13072-021-00422-7
WOS© Times Cited 6
Keyword(s) DNMT inhibitors, 5-Methylcytosine, Mollusks, Invertebrates, Epigenetic inheritance, Epimutation
Abstract

Background

5-Methylcytosine (5mC) is an important epigenetic mark in eukaryotes. Little information about its role exists for invertebrates. To investigate the contribution of 5mC to phenotypic variation in invertebrates, alteration of methylation patterns needs to be produced. Here, we apply new non-nucleoside DNA methyltransferase inhibitors (DNMTi) to introduce aleatory changes into the methylome of mollusk species.

Results

Flavanone inhibitor Flv1 was efficient in reducing 5mC in the freshwater snails Biomphalaria glabrata and Physa acuta, and to a lesser degree, probably due to lower stability in sea water, in the oyster Crassostrea gigas. Flv1 has no toxic effects and significantly decreased the 5mC level in the treated B. glabrata and in its offspring. Drug treatment triggers significant variation in the shell height in both generations. A reduced representation bisulfite-sequencing method called epiGBS corroborates hypomethylation effect of Flv1 in both B. glabrata generations and identifies seven Differential Methylated Regions (DMR) out of 32 found both in Flv1-exposed snails and its progeny, from which 5 were hypomethylated, demonstrating a multigenerational effect. By targeted bisulfite sequencing, we confirmed hypomethylation in a locus and show that it is associated with reduced gene expression.

Conclusions

Flv1 is a new and efficient DNMTi that can be used to induce transient and heritable modifications of the epigenetic landscape and phenotypic traits in mollusks, a phylum of the invertebrates in which epigenetics is understudied.

Full Text
File Pages Size Access
Publisher's official version 25 3 MB Open access
Additional file 1. 158 KB Open access
Top of the page

How to cite 

Luviano Nelia, Lopez Marie, Gawehns Fleur, Chaparro Cristian, Arimondo Paola B., Ivanovic Slavica, David Patrice, Verhoeven Koen, Cosseau Céline, Grunau Christoph (2021). The methylome of Biomphalaria glabrata and other mollusks: enduring modification of epigenetic landscape and phenotypic traits by a new DNA methylation inhibitor. Epigenetics & Chromatin, 14(1), 48 (25p.). Publisher's official version : https://doi.org/10.1186/s13072-021-00422-7 , Open Access version : https://archimer.ifremer.fr/doc/00732/84361/