TY - JOUR
T1 - Epigenetic machinery is functionally conserved in cephalopods
AU - Macchi, Filippo
AU - Edsinger, Eric
AU - Sadler, Kirsten C.
N1 - Funding Information:
We gratefully acknowledge the staff in the Marine Resources Center and Kirsten Peramba for assistance in octopus care and sample collection at the Marine Biological Laboratory and the NYUAD Genomics Core Technology Platform, especially Nizar Drou for assistance with annotating the octopus genome. Patrice Delaney and Catherine Palmer provided assistance with the sample collection, Anjana Ramdas Nair and Patrice Delaney edited the manuscript, and all the members of the Sadler lab and Carrie Albertin provided insightful discussion. We also thank Jan Hsiao and Lola Chenxi Deng for assistance in building the phylogenomic pipeline while at the Salk Institute Chalsani lab.
Funding Information:
Funding was from NIH R21 (MH119646), HFSP Research Program Grant (RGP0060/2017), Vetlesen Foundation Fellowship (to EE), and the NYUAD Faculty Research Fund (to KCS).
Publisher Copyright:
© 2022, The Author(s).
PY - 2022/12
Y1 - 2022/12
N2 - Background: Epigenetic regulatory mechanisms are divergent across the animal kingdom, yet these mechanisms are not well studied in non-model organisms. Unique features of cephalopods make them attractive for investigating behavioral, sensory, developmental, and regenerative processes, and recent studies have elucidated novel features of genome organization and gene and transposon regulation in these animals. However, it is not known how epigenetics regulates these interesting cephalopod features. We combined bioinformatic and molecular analysis of Octopus bimaculoides to investigate the presence and pattern of DNA methylation and examined the presence of DNA methylation and 3 histone post-translational modifications across tissues of three cephalopod species. Results: We report a dynamic expression profile of the genes encoding conserved epigenetic regulators, including DNA methylation maintenance factors in octopus tissues. Levels of 5-methyl-cytosine in multiple tissues of octopus, squid, and bobtail squid were lower compared to vertebrates. Whole genome bisulfite sequencing of two regions of the brain and reduced representation bisulfite sequencing from a hatchling of O. bimaculoides revealed that less than 10% of CpGs are methylated in all samples, with a distinct pattern of 5-methyl-cytosine genome distribution characterized by enrichment in the bodies of a subset of 14,000 genes and absence from transposons. Hypermethylated genes have distinct functions and, strikingly, many showed similar expression levels across tissues while hypomethylated genes were silenced or expressed at low levels. Histone marks H3K27me3, H3K9me3, and H3K4me3 were detected at different levels across tissues of all species. Conclusions: Our results show that the DNA methylation and histone modification epigenetic machinery is conserved in cephalopods, and that, in octopus, 5-methyl-cytosine does not decorate transposable elements, but is enriched on the gene bodies of highly expressed genes and could cooperate with the histone code to regulate tissue-specific gene expression.
AB - Background: Epigenetic regulatory mechanisms are divergent across the animal kingdom, yet these mechanisms are not well studied in non-model organisms. Unique features of cephalopods make them attractive for investigating behavioral, sensory, developmental, and regenerative processes, and recent studies have elucidated novel features of genome organization and gene and transposon regulation in these animals. However, it is not known how epigenetics regulates these interesting cephalopod features. We combined bioinformatic and molecular analysis of Octopus bimaculoides to investigate the presence and pattern of DNA methylation and examined the presence of DNA methylation and 3 histone post-translational modifications across tissues of three cephalopod species. Results: We report a dynamic expression profile of the genes encoding conserved epigenetic regulators, including DNA methylation maintenance factors in octopus tissues. Levels of 5-methyl-cytosine in multiple tissues of octopus, squid, and bobtail squid were lower compared to vertebrates. Whole genome bisulfite sequencing of two regions of the brain and reduced representation bisulfite sequencing from a hatchling of O. bimaculoides revealed that less than 10% of CpGs are methylated in all samples, with a distinct pattern of 5-methyl-cytosine genome distribution characterized by enrichment in the bodies of a subset of 14,000 genes and absence from transposons. Hypermethylated genes have distinct functions and, strikingly, many showed similar expression levels across tissues while hypomethylated genes were silenced or expressed at low levels. Histone marks H3K27me3, H3K9me3, and H3K4me3 were detected at different levels across tissues of all species. Conclusions: Our results show that the DNA methylation and histone modification epigenetic machinery is conserved in cephalopods, and that, in octopus, 5-methyl-cytosine does not decorate transposable elements, but is enriched on the gene bodies of highly expressed genes and could cooperate with the histone code to regulate tissue-specific gene expression.
KW - Cephalopods
KW - DNA methylation
KW - DNMT1
KW - Epigenetics
KW - Histone methylation
KW - Octopus bimaculoides
KW - UHRF1
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U2 - 10.1186/s12915-022-01404-1
DO - 10.1186/s12915-022-01404-1
M3 - Article
C2 - 36104784
AN - SCOPUS:85137925323
SN - 1741-7007
VL - 20
JO - BMC Biology
JF - BMC Biology
IS - 1
M1 - 202
ER -