Proteomics reveals conserved features of histone biology in dinoflagellates

Current knowledge of DNA packaging in eukaryotic nuclei largely centers on its basic unit, the nucleosome. Multiple lineages have, however, diverged from this paradigm, most notably dinoflagellates. Among other molecular oddities, these enigmatic protists have enormous genomes, permanently condensed chromosomes and a foreign gene encoding Dinoflagellate Viral Nucleoprotein (DVNP), which is used for packing DNA. Some dinoflagellates also have Histone-like Proteins (HLPs) acquired from bacteria via lateral gene transfer. Dinoflagellates were long thought to lack histones entirely, but canonical histone genes have been identified by transcriptomics. Here, we performed proteomics on purified nuclei and confirmed the presence of all four core histone classes, along with variants, and DVNP in the dinoflagellates Oxyrrhis marina and Amphidinium carterae and HLPs in A. carterae . We also identified putative histone post-translational modifications found in canonical eukaryotes. Comparative genomics of dinoflagellates revealed histone-handling and modification machinery alongside an apparent reduction in, or diversification of, machinery responsible for replication-dependent nucleosome deposition (CAF-1), consistent with a predominantly transcription-associated role for nucleosomes. Furthermore, proteomics revealed modifications of DVNP and HLP, raising the possibility of machinery co-opting. These observations support a new model of a dinoflagellate chromatin that includes the localization of canonical nucleosomes to insulated chromatin territories (INTs).