Conservation and divergence of the histone code in nucleomorphs

Abstract

Background: Nucleomorphs, the remnant nuclei of photosynthetic algae that have become endosymbionts to other eukaryotes, represent a unique example of convergent reductive genome evolution in eukaryotes, having evolved independently on two separate occasions in chlorarachniophytes and cryptophytes. The nucleomorphs of the two groups have evolved in a remarkably convergent manner, with numerous very similar features. Chief among them is the extreme reduction and compaction of nucleomorph genomes, with very small chromosomes and extremely short or even completely absent intergenic spaces. These characteristics pose a number of intriguing questions regarding the mechanisms of transcription and gene regulation in such a crowded genomic context, in particular in terms of the functioning of the histone code, which is common to almost all eukaryotes and plays a central role in chromatin biology.

Results: This study examines the sequences of nucleomorph histone proteins in order to address these issues. Remarkably, all classical transcription- and repression-related components of the histone code seem to be missing from chlorarachniophyte nucleomorphs. Cryptophyte nucleomorph histones are generally more similar to the conventional eukaryotic state; however, they also display significant deviations from the typical histone code. Based on the analysis of specific components of the code, we discuss the state of chromatin and the transcriptional machinery in these nuclei.

Conclusions: The results presented here shed new light on the mechanisms of nucleomorph transcription and gene regulation and provide a foundation for future studies of nucleomorph chromatin and transcriptional biology.

Keywords: Chromatin; Histone code; Histones; Nucleomorphs; Transcription.

Fig. 1

Multiple seqience alignment of chlorarachniophyte nucleomorph histones H3 and nuclear H3 histones from several representative eukaryotes. Multiple sequence alignments were carried out using MUSCLE [102] and visualized using Jalview [103]

Fig. 2

Multiple seqience alignment of chlorarachniophyte nucleomorph histones H4 and nuclear H4 histones from several representative eukaryotes. Multiple sequence alignments were carried out using MUSCLE [102] and visualized using Jalview [103]

Fig. 3

Multiple seqience alignment of cryptophyte nucleomorph histones H3 and nuclear H3 histones from several representative eukaryotes. Multiple sequence alignments were carried out using MUSCLE [102] and visualized using Jalview [103]

Fig. 4

Multiple seqience alignment of cryptophyte nucleomorph histones H4 and nuclear H4 histones from several representative eukaryotes. Multiple sequence alignments were carried out using MUSCLE [102] and visualized using Jalview [103]

Fig. 5

Conservation of key posttranscriptionally modified residues in chlorarachniophyte and cryptophyte nucleomorph histones H3 and H4. a Histone H3; b Histone H4. The radius r refers to the size of the context considered when scoring conservation. When r=1, only the residue itself is considered; when r=0, a perfect match to the three-amino acid peptide also including the flanking residues on each side is required; when r=2, the five-amino acid peptide also including the two flanking residues on each side is considered. A score of 1 means conservation according to these criteria, while a score of 0 means lack of conservation. Conservation was scored against the Homo sapiens histone H3.3 and H4 sequences