Distinctive Nuclear Features of Dinoflagellates with A Particular Focus on Histone and Histone-Replacement Proteins

Abstract

Dinoflagellates are important eukaryotic microorganisms that play critical roles as producers and grazers, and cause harmful algal blooms. The unusual nuclei of dinoflagellates “dinokaryon” have led researchers to investigate their enigmatic nuclear features. Their nuclei are unusual in terms of their permanently condensed nucleosome-less chromatin, immense genome, low protein to DNA ratio, guanine-cytosine rich methylated DNA, and unique mitosis process. Furthermore, dinoflagellates are the only known group of eukaryotes that apparently lack histone proteins. Over the course of evolution, dinoflagellates have recruited other proteins, e.g., histone-like proteins (HLPs), from bacteria and dinoflagellates/viral nucleoproteins (DVNPs) from viruses as histone substitutes. Expression diversity of these nucleoproteins has greatly influenced the chromatin structure and gene expression regulation in dinoflagellates. Histone replacement proteins (HLPs and DVNPs) are hypothesized to perform a few similar roles as histone proteins do in other eukaryotes, i.e., gene expression regulation and repairing DNA. However, their role in bulk packaging of DNA is not significant as low amounts of proteins are associated with the gigantic genome. This review intends to summarize the discoveries encompassing unique nuclear features of dinoflagellates, particularly focusing on histone and histone replacement proteins. In addition, a comprehensive view of the evolution of dinoflagellate nuclei is presented.

Genetic and spatial organization of the unusual chromosomes of the dinoflagellate Symbiodinium microadriaticum

“…However, only a very small fraction of the genome is nucleosomal, as shown, for example, by nuclease digestion patterns 19 . DNA is likely packaged by other proteins, for example histone-like proteins and dinoflagellate/ viral nuclear proteins (DVNPs) derived from bacteria and viruses, respectively [19][20][21] . Dinoflagellate chromosomes appear permanently condensed throughout the cell cycle, and optical birefringence properties of chromosomes suggest they have liquid-crystalline features 22 .…”

Chromosome-scale assembly of the coral endosymbiontSymbiodinium microadriaticumgenome provides insight into the unique biology of dinoflagellate chromosomes

“…Alternatively, the telomeric domains may differ in their association with other DNA condensing proteins such as histone-like proteins 61,62 .…”

“…Histones are replaced by other basic proteins, e.g. histone-like proteins derived from bacteria and dinoflagellates/viral nucleoproteins (DVNPs) derived from viruses 20,61,63 .…”

Nuclear Gene Transformation in the Dinoflagellate Oxyrrhis marina

“…It is an established model species for both ecological and evolutionary research due to its easy cultivable nature, extensive studies related to feeding behavior and nutrition, and its position in dinoflagellate phylogeny [38][39][40][41][42]. As an early branching dinoflagellate, O. marina is not considered a "core" dinoflagellate [13,[43][44][45]. Although it retains more typical eukaryotic features that are lacking in later diverging dinoflagellate taxa, it still shares many of the peculiar biological characteristics of the "core" dinoflagellates (e.g., trans-splicing, permanently condensed chromosomes, the use of DVNPs, fragmented mitochondrial genome, large genome) [16,44,45]; thus, it represents a good model for understanding dinoflagellate evolution [38][39][40][41][42][43][44][45][46].…”

“…As an early branching dinoflagellate, O. marina is not considered a "core" dinoflagellate [13,[43][44][45]. Although it retains more typical eukaryotic features that are lacking in later diverging dinoflagellate taxa, it still shares many of the peculiar biological characteristics of the "core" dinoflagellates (e.g., trans-splicing, permanently condensed chromosomes, the use of DVNPs, fragmented mitochondrial genome, large genome) [16,44,45]; thus, it represents a good model for understanding dinoflagellate evolution [38][39][40][41][42][43][44][45][46]. In addition, O. marina has represented planktonic heterotrophs in experiments examining both how they feed and their nutritional value [47][48][49].…”