Environmentally induced DNA methylation is inherited across generations in an aquatic keystone species

Nathalie Feiner; Reinder Radersma; Louella Vasquez; Markus Ringnér; Björn Nystedt; Amanda Raine; Elmar W. Tobi; Bastiaan T. Heijmans; Tobias Uller

doi:10.1016/j.isci.2022.104303

Environmentally induced DNA methylation is inherited across generations in an aquatic keystone species

Nathalie Feiner^*, Reinder Radersma, Louella Vasquez, Markus Ringnér, Björn Nystedt, Amanda Raine, Elmar W. Tobi, Bastiaan T. Heijmans, Tobias Uller^*

^*Corresponding author for this work

Obstetrics & Gynecology

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

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Abstract

Transgenerational inheritance of environmentally induced epigenetic marks can have significant impacts on eco-evolutionary dynamics, but the phenomenon remains controversial in ecological model systems. We used whole-genome bisulfite sequencing of individual water fleas (Daphnia magna) to assess whether environmentally induced DNA methylation is transgenerationally inherited. Genetically identical females were exposed to one of three natural stressors, or a de-methylating drug, and their offspring were propagated clonally for four generations under control conditions. We identified between 70 and 225 differentially methylated CpG positions (DMPs) in F1 individuals whose mothers were exposed to a natural stressor. Roughly half of these environmentally induced DMPs persisted until generation F4. In contrast, treatment with the drug demonstrated that pervasive hypomethylation upon exposure is reset almost completely after one generation. These results suggest that environmentally induced DNA methylation is non-random and stably inherited across generations in Daphnia, making epigenetic inheritance a putative factor in the eco-evolutionary dynamics of freshwater communities.

Original language	English
Article number	104303
Journal	iScience
Volume	25
Issue number	5
Early online date	25 Apr 2022
DOIs	https://doi.org/10.1016/j.isci.2022.104303
Publication status	Published - 20 May 2022

Bibliographical note

Funding Information:
This work was supported by the John Templeton Foundation ( #60501 ) and the SciLifeLab Bioinformatics Long-term Support (both to T.U.), the Knut and Alice Wallenberg Foundation through a Wallenberg Academy Fellowship to T.U., and the European and Swedish Research Councils through Starting Grants ( #948126 and #2020-03650 ) to N.F. L.V., M.R. The Knut and Alice Wallenberg Foundation financially supported L.V., M.R. and B.N. as part of the National Bioinformatics Infrastructure Sweden at SciLifeLab. Sequencing was performed by the SNP&SEQ Technology Platform, which is part of the National Genomics Infrastructure ( NGI ) hosted by SciLifeLab in Uppsala, Sweden. NGI is supported by grants from the Swedish Research Council and the Knut and Alice Wallenberg Foundation . The genomic analyses were enabled by resources provided by the Swedish National Infrastructure for Computing ( SNIC ) at UPPMAX, partially funded by the Swedish Research Council through grant agreement no. # 2018-05973 .

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© 2022 The Author(s)

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Environmentally induced DNA methylation is inherited across generations in an aquatic keystone speciesFinal published version, 3.87 MBLicence: CC BY

Cite this

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title = "Environmentally induced DNA methylation is inherited across generations in an aquatic keystone species",

abstract = "Transgenerational inheritance of environmentally induced epigenetic marks can have significant impacts on eco-evolutionary dynamics, but the phenomenon remains controversial in ecological model systems. We used whole-genome bisulfite sequencing of individual water fleas (Daphnia magna) to assess whether environmentally induced DNA methylation is transgenerationally inherited. Genetically identical females were exposed to one of three natural stressors, or a de-methylating drug, and their offspring were propagated clonally for four generations under control conditions. We identified between 70 and 225 differentially methylated CpG positions (DMPs) in F1 individuals whose mothers were exposed to a natural stressor. Roughly half of these environmentally induced DMPs persisted until generation F4. In contrast, treatment with the drug demonstrated that pervasive hypomethylation upon exposure is reset almost completely after one generation. These results suggest that environmentally induced DNA methylation is non-random and stably inherited across generations in Daphnia, making epigenetic inheritance a putative factor in the eco-evolutionary dynamics of freshwater communities.",

author = "Nathalie Feiner and Reinder Radersma and Louella Vasquez and Markus Ringn{\'e}r and Bj{\"o}rn Nystedt and Amanda Raine and Tobi, {Elmar W.} and Heijmans, {Bastiaan T.} and Tobias Uller",

note = "Funding Information: This work was supported by the John Templeton Foundation ( #60501 ) and the SciLifeLab Bioinformatics Long-term Support (both to T.U.), the Knut and Alice Wallenberg Foundation through a Wallenberg Academy Fellowship to T.U., and the European and Swedish Research Councils through Starting Grants ( #948126 and #2020-03650 ) to N.F. L.V., M.R. The Knut and Alice Wallenberg Foundation financially supported L.V., M.R. and B.N. as part of the National Bioinformatics Infrastructure Sweden at SciLifeLab. Sequencing was performed by the SNP&SEQ Technology Platform, which is part of the National Genomics Infrastructure ( NGI ) hosted by SciLifeLab in Uppsala, Sweden. NGI is supported by grants from the Swedish Research Council and the Knut and Alice Wallenberg Foundation . The genomic analyses were enabled by resources provided by the Swedish National Infrastructure for Computing ( SNIC ) at UPPMAX, partially funded by the Swedish Research Council through grant agreement no. # 2018-05973 . Publisher Copyright: {\textcopyright} 2022 The Author(s)",

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AU - Tobi, Elmar W.

AU - Heijmans, Bastiaan T.

AU - Uller, Tobias

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N2 - Transgenerational inheritance of environmentally induced epigenetic marks can have significant impacts on eco-evolutionary dynamics, but the phenomenon remains controversial in ecological model systems. We used whole-genome bisulfite sequencing of individual water fleas (Daphnia magna) to assess whether environmentally induced DNA methylation is transgenerationally inherited. Genetically identical females were exposed to one of three natural stressors, or a de-methylating drug, and their offspring were propagated clonally for four generations under control conditions. We identified between 70 and 225 differentially methylated CpG positions (DMPs) in F1 individuals whose mothers were exposed to a natural stressor. Roughly half of these environmentally induced DMPs persisted until generation F4. In contrast, treatment with the drug demonstrated that pervasive hypomethylation upon exposure is reset almost completely after one generation. These results suggest that environmentally induced DNA methylation is non-random and stably inherited across generations in Daphnia, making epigenetic inheritance a putative factor in the eco-evolutionary dynamics of freshwater communities.

AB - Transgenerational inheritance of environmentally induced epigenetic marks can have significant impacts on eco-evolutionary dynamics, but the phenomenon remains controversial in ecological model systems. We used whole-genome bisulfite sequencing of individual water fleas (Daphnia magna) to assess whether environmentally induced DNA methylation is transgenerationally inherited. Genetically identical females were exposed to one of three natural stressors, or a de-methylating drug, and their offspring were propagated clonally for four generations under control conditions. We identified between 70 and 225 differentially methylated CpG positions (DMPs) in F1 individuals whose mothers were exposed to a natural stressor. Roughly half of these environmentally induced DMPs persisted until generation F4. In contrast, treatment with the drug demonstrated that pervasive hypomethylation upon exposure is reset almost completely after one generation. These results suggest that environmentally induced DNA methylation is non-random and stably inherited across generations in Daphnia, making epigenetic inheritance a putative factor in the eco-evolutionary dynamics of freshwater communities.

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Environmentally induced DNA methylation is inherited across generations in an aquatic keystone species

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