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Eukaryotic core histone diversification in light of the histone doublet and DNA topo II genes of Marseilleviridae

Albert J. Erives
doi: https://doi.org/10.1101/022236
Albert J. Erives
Department of Biology, University of Iowa, Iowa City, IA 52242-1324, USA
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Abstract

While eukaryotic and archaean genomes encode the histone fold domain, only eukaryotes encode the core histones H2A, H2B, H3, and H4. Core histones assemble into a hetero-octamer rather than the homo-tetramer of Archaea. Thus it was unexpected that core histone “doublets” were identified in the cytoplasmic replication factories of the Marseilleviridae (MV), one family of Nucleo-Cytoplasmic Large DNA Viruses (NCLDV). Here we analyze the core histone doublet genes from all known Marseilleviridae genomes and show that they encode obligate H2B-H2A and H4-H3 dimers of likely proto-eukaryotic origin. Each MV core histone moiety forms a sister clade to a eukaryotic core histone clade inclusive of canonical core histone paralogs, suggesting that MV core histone moieties diverged prior to eukaryotic neofunctionalizations associated with paired linear chromosomes and variant histone octamer assembly. We also show that all MV genomes encode a eukaryote-like DNA topoisomerase II enzyme that forms a clade that is sister to the eukaryotic clade. As DNA topo II influences histone deposition and chromatin compaction and is the second most abundant nuclear protein after histones, we suggest MV genes underlie a proto-chromatinized replisome that diverged prior to diversification of eukaryotic core histone variants. Thus, combined domain architecture and phylogenomic analyses suggest that a primitive origin for MV chromatin genes is a more parsimonious explanation than horizontal gene transfers + gene fusions + long-branch attraction constrained to each core histone clade. These results imply that core histones were utilized ancestrally in viral DNA compaction, protection from host endonucleases, and/or other unknown processes associated with NCLDV-like progenitors.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted July 08, 2015.
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Eukaryotic core histone diversification in light of the histone doublet and DNA topo II genes of Marseilleviridae
Albert J. Erives
bioRxiv 022236; doi: https://doi.org/10.1101/022236
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Eukaryotic core histone diversification in light of the histone doublet and DNA topo II genes of Marseilleviridae
Albert J. Erives
bioRxiv 022236; doi: https://doi.org/10.1101/022236

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