Comparative analysis of genome-scale, base-resolution DNA methylation profiles across 580 animal species

Johanna Klughammer; Daria Romanovskaia; Amelie Nemc; Annika Posautz; Charlotte A. Seid; Linda C. Schuster; Melissa C. Keinath; Juan Sebastian Lugo Ramos; Lindsay Kosack; Ann Evankow; Dieter Printz; Stefanie Kirchberger; Bekir Ergüner; Paul Datlinger; N Fortelny; Christian Schmidl; Matthias Farlik; Kaja Skjærven; Andreas Bergthaler; Miriam Liedvogel; Denise Thaller; Pamela A. Burger; Marcella Hermann; Martin Distel; Daniel L. Distel; Anna Kübber-Heiss; Christoph Bock

doi:10.1038/s41467-022-34828-y

Comparative analysis of genome-scale, base-resolution DNA methylation profiles across 580 animal species

Johanna Klughammer^*, Daria Romanovskaia, Amelie Nemc, Annika Posautz, Charlotte A. Seid, Linda C. Schuster, Melissa C. Keinath, Juan Sebastian Lugo Ramos, Lindsay Kosack, Ann Evankow, Dieter Printz, Stefanie Kirchberger, Bekir Ergüner, Paul Datlinger, N Fortelny, Christian Schmidl, Matthias Farlik, Kaja Skjærven, Andreas Bergthaler, Miriam LiedvogelDenise Thaller, Pamela A. Burger, Marcella Hermann, Martin Distel, Daniel L. Distel, Anna Kübber-Heiss, Christoph Bock^*

^*Corresponding author for this work

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

Abstract

Methylation of cytosines is a prototypic epigenetic modification of the DNA. It has been implicated in various regulatory mechanisms across the animal kingdom and particularly in vertebrates. We mapped DNA methylation in 580 animal species (535 vertebrates, 45 invertebrates), resulting in 2443 genome-scale DNA methylation profiles of multiple organs. Bioinformatic analysis of this large dataset quantified the association of DNA methylation with the underlying genomic DNA sequence throughout vertebrate evolution. We observed a broadly conserved link with two major transitions—once in the first vertebrates and again with the emergence of reptiles. Cross-species comparisons focusing on individual organs supported a deeply conserved association of DNA methylation with tissue type, and cross-mapping analysis of DNA methylation at gene promoters revealed evolutionary changes for orthologous genes. In summary, this study establishes a large resource of vertebrate and invertebrate DNA methylomes, it showcases the power of reference-free epigenome analysis in species for which no reference genomes are available, and it contributes an epigenetic perspective to the study of vertebrate evolution.

Original language	English
Article number	232
Number of pages	23
Journal	Nature Communications
Volume	2023
Issue number	14
DOIs	https://doi.org/10.1038/s41467-022-34828-y
Publication status	Published - 16 Jan 2023

Keywords

Epigenomics
Gene Regulatory Networks
Genome evolution

Fields of Science and Technology Classification 2012

106 Biology

Access to Document

10.1038/s41467-022-34828-y

Cite this

Klughammer, J., Romanovskaia, D., Nemc, A., Posautz, A., Seid, C. A., Schuster, L. C., Keinath, M. C., Lugo Ramos, J. S., Kosack, L., Evankow, A., Printz, D., Kirchberger, S., Ergüner, B., Datlinger, P., Fortelny, N., Schmidl, C., Farlik, M., Skjærven, K., Bergthaler, A., ... Bock, C. (2023). Comparative analysis of genome-scale, base-resolution DNA methylation profiles across 580 animal species. Nature Communications, 2023(14), Article 232. https://doi.org/10.1038/s41467-022-34828-y

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title = "Comparative analysis of genome-scale, base-resolution DNA methylation profiles across 580 animal species",

abstract = "Methylation of cytosines is a prototypic epigenetic modification of the DNA. It has been implicated in various regulatory mechanisms across the animal kingdom and particularly in vertebrates. We mapped DNA methylation in 580 animal species (535 vertebrates, 45 invertebrates), resulting in 2443 genome-scale DNA methylation profiles of multiple organs. Bioinformatic analysis of this large dataset quantified the association of DNA methylation with the underlying genomic DNA sequence throughout vertebrate evolution. We observed a broadly conserved link with two major transitions—once in the first vertebrates and again with the emergence of reptiles. Cross-species comparisons focusing on individual organs supported a deeply conserved association of DNA methylation with tissue type, and cross-mapping analysis of DNA methylation at gene promoters revealed evolutionary changes for orthologous genes. In summary, this study establishes a large resource of vertebrate and invertebrate DNA methylomes, it showcases the power of reference-free epigenome analysis in species for which no reference genomes are available, and it contributes an epigenetic perspective to the study of vertebrate evolution.",

keywords = "Epigenomics, Gene Regulatory Networks, Genome evolution",

author = "Johanna Klughammer and Daria Romanovskaia and Amelie Nemc and Annika Posautz and Seid, {Charlotte A.} and Schuster, {Linda C.} and Keinath, {Melissa C.} and {Lugo Ramos}, {Juan Sebastian} and Lindsay Kosack and Ann Evankow and Dieter Printz and Stefanie Kirchberger and Bekir Erg{\"u}ner and Paul Datlinger and N Fortelny and Christian Schmidl and Matthias Farlik and Kaja Skj{\ae}rven and Andreas Bergthaler and Miriam Liedvogel and Denise Thaller and Burger, {Pamela A.} and Marcella Hermann and Martin Distel and Distel, {Daniel L.} and Anna K{\"u}bber-Heiss and Christoph Bock",

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doi = "10.1038/s41467-022-34828-y",

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Klughammer, J, Romanovskaia, D, Nemc, A, Posautz, A, Seid, CA, Schuster, LC, Keinath, MC, Lugo Ramos, JS, Kosack, L, Evankow, A, Printz, D, Kirchberger, S, Ergüner, B, Datlinger, P, Fortelny, N, Schmidl, C, Farlik, M, Skjærven, K, Bergthaler, A, Liedvogel, M, Thaller, D, Burger, PA, Hermann, M, Distel, M, Distel, DL, Kübber-Heiss, A & Bock, C 2023, 'Comparative analysis of genome-scale, base-resolution DNA methylation profiles across 580 animal species', Nature Communications, vol. 2023, no. 14, 232. https://doi.org/10.1038/s41467-022-34828-y

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T1 - Comparative analysis of genome-scale, base-resolution DNA methylation profiles across 580 animal species

AU - Klughammer, Johanna

AU - Romanovskaia, Daria

AU - Nemc, Amelie

AU - Posautz, Annika

AU - Seid, Charlotte A.

AU - Schuster, Linda C.

AU - Keinath, Melissa C.

AU - Lugo Ramos, Juan Sebastian

AU - Kosack, Lindsay

AU - Evankow, Ann

AU - Printz, Dieter

AU - Kirchberger, Stefanie

AU - Ergüner, Bekir

AU - Datlinger, Paul

AU - Fortelny, N

AU - Schmidl, Christian

AU - Farlik, Matthias

AU - Skjærven, Kaja

AU - Bergthaler, Andreas

AU - Liedvogel, Miriam

AU - Thaller, Denise

AU - Burger, Pamela A.

AU - Hermann, Marcella

AU - Distel, Martin

AU - Distel, Daniel L.

AU - Kübber-Heiss, Anna

AU - Bock, Christoph

PY - 2023/1/16

Y1 - 2023/1/16

N2 - Methylation of cytosines is a prototypic epigenetic modification of the DNA. It has been implicated in various regulatory mechanisms across the animal kingdom and particularly in vertebrates. We mapped DNA methylation in 580 animal species (535 vertebrates, 45 invertebrates), resulting in 2443 genome-scale DNA methylation profiles of multiple organs. Bioinformatic analysis of this large dataset quantified the association of DNA methylation with the underlying genomic DNA sequence throughout vertebrate evolution. We observed a broadly conserved link with two major transitions—once in the first vertebrates and again with the emergence of reptiles. Cross-species comparisons focusing on individual organs supported a deeply conserved association of DNA methylation with tissue type, and cross-mapping analysis of DNA methylation at gene promoters revealed evolutionary changes for orthologous genes. In summary, this study establishes a large resource of vertebrate and invertebrate DNA methylomes, it showcases the power of reference-free epigenome analysis in species for which no reference genomes are available, and it contributes an epigenetic perspective to the study of vertebrate evolution.

AB - Methylation of cytosines is a prototypic epigenetic modification of the DNA. It has been implicated in various regulatory mechanisms across the animal kingdom and particularly in vertebrates. We mapped DNA methylation in 580 animal species (535 vertebrates, 45 invertebrates), resulting in 2443 genome-scale DNA methylation profiles of multiple organs. Bioinformatic analysis of this large dataset quantified the association of DNA methylation with the underlying genomic DNA sequence throughout vertebrate evolution. We observed a broadly conserved link with two major transitions—once in the first vertebrates and again with the emergence of reptiles. Cross-species comparisons focusing on individual organs supported a deeply conserved association of DNA methylation with tissue type, and cross-mapping analysis of DNA methylation at gene promoters revealed evolutionary changes for orthologous genes. In summary, this study establishes a large resource of vertebrate and invertebrate DNA methylomes, it showcases the power of reference-free epigenome analysis in species for which no reference genomes are available, and it contributes an epigenetic perspective to the study of vertebrate evolution.

KW - Epigenomics

KW - Gene Regulatory Networks

KW - Genome evolution

U2 - 10.1038/s41467-022-34828-y

DO - 10.1038/s41467-022-34828-y

M3 - Article

C2 - 36646694

SN - 2041-1723

VL - 2023

JO - Nature Communications

JF - Nature Communications

IS - 14

M1 - 232

ER -