A species-specific nucleosomal signature defines a periodic distribution of amino acids in proteins

Abstract

Nucleosomes are the basic structural units of chromatin. Most of the yeast genome is organized in a pattern of positioned nucleosomes that is stably maintained under a wide range of physiological conditions. In this work, we have searched for sequence determinants associated with positioned nucleosomes in four species of fission and budding yeasts. We show that mononucleosomal DNA follows a highly structured base composition pattern, which differs among species despite the high degree of histone conservation. These nucleosomal signatures are present in transcribed and non-transcribed regions across the genome. In the case of open reading frames, they correctly predict the relative distribution of codons on mononucleosomal DNA, and they also determine a periodicity in the average distribution of amino acids along the proteins. These results establish a direct and species-specific connection between the position of each codon around the histone octamer and protein composition.

Nucleosomal signatures impose nucleosome positioning in coding and noncoding sequences in the genome

“…These differences are consistent with the phylogenetic distance of 119, 221, and 350 million years of S. octosporus, S. japonicus and S. cerevisiae, respectively, relative to S. pombe Hoffman et al 2015) and with the fact that the nucleosomal signatures are more similar between S. octosporus and S. pombe than between S. japonicus and S. pombe ( Fig. 5; Quintales et al 2015a). It is currently unknown whether these small differences in the histone octamer could be responsible for the different affinity of nucleosomes of different organisms for the same DNA sequence or whether other factors like histone concentration, the linker-tocore histone ratio, or other thermodynamic or biophysical parameters could be involved (Beshnova et al 2014).…”

“…6D, dotted trace) confirmed this result and showed that, in some cases, internucleosomal positions in S. cerevisiae coincided with dyad positions in S. pombe. This could be due to the fact that A + T-rich sequences are preferentially found at the dyad and linker regions in S. pombe and S. cerevisiae, respectively (Tillo and Hughes 2009;Moyle-Heyrman et al 2013;Quintales et al 2015a). …”

“…They are present in transcribed and nontranscribed regions and vary widely even among species of the same genus (Quintales et al 2015a). In this work, we have analyzed whether nucleosomal signatures contain information capable of targeting nucleosomes to specific positions in natural and synthetic DNA molecules integrated into the genome.…”

“…S4) suggests the intriguing possibility that, in addition to modulating the stability of mRNA and its rate of translation (Plotkin and Kudla 2011;Presnyak et al 2015), the distribution of synonymous codons might also contribute to nucleosome positioning along ORFs. Nucleosomal signatures have a strong impact in genome and protein evolution to the extent that, in the case of coding regions, they correctly predict the relative distribution of the 20 amino acids along proteins based on the position of the corresponding codons along mononucleosomal DNA (Warnecke et al 2008;Quintales et al 2015a).…”

“…However, it was not immediately obvious how to design such sequences given the expected degeneracy of the putative sequence determinants. Despite the large variability among the thousands of mononucleosomal sequences in the genome, their aggregated profiles generate well-defined patterns in the distribution of the four nucleotides that we have called nucleosomal signatures (Quintales et al 2015a). We hypothesized that the information contained within these signatures could contribute to nucleosome positioning, and therefore, we used them as a starting point in the design of the synthetic DNA sequences.…”