Abstract
Within canonical eukaryotic nuclei, DNA is packaged with highly conserved histone proteins into nucleosomes, which facilitate DNA condensation and contribute to genomic regulation. Yet the dinoflagellates, a group of unicellular algae, are a striking exception to this otherwise universal feature as they have largely abandoned histones and acquired apparently viral-derived substitutes termed DVNPs (dinoflagellate-viral-nucleoproteins). Despite the magnitude of this transition, its evolutionary drivers remain unknown. Here, using Saccharomyces cerevisiae as a model, we show that DVNP impairs growth and antagonizes chromatin by localizing to histone binding sites, displacing nucleosomes, and impairing transcription. Furthermore, DVNP toxicity can be relieved through histone depletion and cells diminish their histones in response to DVNP expression suggesting that histone reduction could have been an adaptive response to these viral proteins. These findings provide insights into eukaryotic chromatin evolution and highlight the potential for horizontal gene transfer to drive the divergence of cellular systems.
Highlights
Within canonical eukaryotic nuclei, DNA is packaged with highly conserved histone proteins into nucleosomes, which facilitate DNA condensation and contribute to genomic regulation
SV40 nuclear localization signals (NLS) and or three hemaglutinin (3HA) epitope tags were added to the N-terminus or C-terminus and protein expression was confirmed by immunoblot following galactose induction (Fig. 1a, b)
Immunofluorescence revealed co-localization between DVNP and Hoescht stain with all constructs, suggesting that DVNP localized to the nucleus independent of the additional NLS (Fig. 1c).We noted DVNP-dense regions associated with the nucleus (Fig. 1c)
Summary
DNA is packaged with highly conserved histone proteins into nucleosomes, which facilitate DNA condensation and contribute to genomic regulation. DVNP toxicity can be relieved through histone depletion and cells diminish their histones in response to DVNP expression suggesting that histone reduction could have been an adaptive response to these viral proteins These findings provide insights into eukaryotic chromatin evolution and highlight the potential for horizontal gene transfer to drive the divergence of cellular systems. To circumvent the limitations associated with dinoflagellates and gain insights into the initial transition between histone and DVNPbased chromatin, we employed an experimental evolutionary approach utilizing S. cerevisiae to assess how DVNP interacts with canonical eukaryotic chromatin To this end, we found that DVNP antagonizes chromatin by localizing to histone binding sites, displacing nucleosomes, impairing transcription, and inhibiting growth. These results reveal that histone depletion is an adaptive response to DVNP and emphasize the role that horizontal gene transfer, and possibly pathogenic stresses, can play in driving cellular evolution
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