Comparative genomics illuminates adaptive evolution of DVNP with lifestyle and with loss of histone H1 in dinoflagellates

Abstract

About ten years ago dinoflagellate/viral nucleoprotein (DVNP) was discovered in dinoflagellates, an ecologically important and evolutionarily enigmatic group of aquatic protists. Apparently acquired from a viral origin, the appearance of DVNP coincided with the loss of nucleosome, a rare event in eukaryote evolution. Despite the potential importance of DVNP as the substitute of histones, its evolutionary trajectory and adaptive significance remain elusive. Here, we conducted comparative analyses using existing dinoflagellate genomes and transcriptomes from 26 species ranging from ancestral to later-diverging lineages to investigate the pattern of sequence and structural divergence. Results showed that the functional domestication of DVNP in ancestral dinoflagellates coincided with the loss of histone H1, while subsequent DVNP differentiation was accompanied by the yet another genomic innovation: acquisition of bacterial-originated histone-like protein. Furthermore, our data split DVNP into two major groups: the core DVNP that resembles histone H1 and shows consistently high levels of expression and the non-core DVNP with higher sequence variability and showing lower yet variable levels of expression. In addition, we observed a trend in DVNP evolution tracing that in lifestyle differentiation. This work offers insights into the adaptive evolution of DVNP, laying the foundation for further inquiries of evolutionary drivers and functional innovation of DVNP to enhance our understanding of dinoflagellate evolution and ecological success.