Archaeal histone selection of nucleosome positioning sequences and the procaryotic origin of histone-dependent genome evolution

Archaeal histones and the eucaryal (eucaryotic) nucleosome core histones ha ve almost identical histone folds. Here, we show that DNA molecules selecti vely incorporated by rHMfB (recombinant archaeal histone B from Methanother mus fervidus) into archaeal nucleosomes from a mixture of similar to 10(14) random sequence molecules contain sequence motifs shown previously to dire ct eucaryal nucleosome positioning. The dinucleotides GC, AA (=TT) and TA a re repeated at similar to 10 bp intervals, with the GC harmonic displaced s imilar to5 bp from the AA and TA harmonics [(GCN(3),AA or TA)(n)]. AT and C G were not strongly selected, indicating that TA not equal AT and GC not eq ual CG in terms of facilitating archaeal nucleosome assembly. The selected molecules have affinities for rHMfB ranging from similar to9 to 18-fold hig her than the level of affinity of the starting population, and direct the p ositioned assembly of archaeal nucleosomes. Fourier-transform analyses have revealed that AA dinucleotides are much enriched at similar to 10.1 bp int ervals, the helical repeat of DNA wrapped around a nucleosome, in the genom es of Eucarya and the histone-containing Euryarchaeota, but not in the geno mes of Bacterin and Crenarchaeota, procaryotes that do not have histones. F acilitating histone packaging of genomic DNA has apparently therefore impos ed constraints on genome sequence evolution, and since archaeal histones ha ve no structure in addition to the histone fold, these constraints must res ult predominantly from histone fold-DNA contacts. Based on the three-domain universal phylogeny, histones and histone-dependent genome sequence evolut ion most likely evolved after the bacterial-archaeal divergence but before the archaeal-eucaryal divergence, and were subsequently lost in the Crenarc haeota. However, with lateral gene transfer, the first histone fold could a lternatively have evolved after the archaeal-eucaryal divergence, early in either the euryarchaeal or eucaryal lineages. (C) 2000 Academic Press.