Chloroplast protein and centrosomal genes, a tRNA intron, and odd telomeres in an unusually compact eukaryotic genome, the cryptomonad nucleomorph

Cells of several major algal groups are evolutionary chimeras of two radica lly different eukaryotic cells. Most of these "cells within cells" lost the nucleus of the former algal endosymbiont. But after hundreds of millions o f years cryptomonads still retain the nucleus of their former red algal end osymbiont as a tiny relict organelle, the nucleomorph, which has three minu te linear chromosomes, but their function and the nature of their ends have been unclear. We report extensive cryptomonad nucleomorph sequences (68.5 kb), from one end of each of the three chromosomes of Guillardia theta. Tel omeres of the nucleomorph chromosomes differ dramatically from those of oth er eukaryotes, being repeats of the 23-mer sequence (AG)(7)AAG(6)A, not a t ypical hexamer (commonly TTAGGG). The subterminal regions comprising the rR NA cistrons and one protein-coding gene are exactly repeated at all three c hromosome ends. Gene density (one per 0.8 kb) is the highest for any cellul ar genome. None of the 38 protein-coding genes has spliceosomal introns, in marked contrast to the chlorarachniophyte nucleomorph. Most identified nuc leomorph genes are for gene expression or protein degradation; histone, tub ulin, and putatively centrosomal ranbpm genes are probably important for ch romosome segregation. No genes for primary or secondary metabolism have bee n found. Two of the three tRNA genes have introns, one in a hitherto undesc ribed location. Intergenic regions are exceptionally short; three genes tra nscribed by two different RNA polymerases overlap their neighbors. The repo rted sequences encode two essential chloroplast proteins, FtsZ and rubredox in, thus explaining why cryptomonad nucleomorphs persist.