The highly reduced genome of an enslaved algal nucleus

Chromophyte algae differ fundamentally from plants in possessing chloroplas ts that contain chlorophyll c and that have a more complex bounding-membran e topology(1). Although chromophytes are known to be evolutionary chimaeras of a red alga and a non-photosynthetic host(1), which gave rise to their e xceptional membrane complexity, their cell biology is poorly understood. Cr yptomonads are the only chromophytes that still retain the enslaved red alg al nucleus as a minute nucleomorph(2-4). Here we report complete sequences for all three nucleomorph chromosomes from the cryptomonad Guillardia theta . This tiny 551-kilobase eukaryotic genome is the most gene-dense known, wi th only 17 diminutive spliceosomal introns and 44 overlapping genes. Marked evolutionary compaction hundreds of millions of years ago(1,4,5) eliminate d nearly all the nucleomorph genes for metabolic functions, but left 30 for chloroplast-located proteins. To allow expression of these proteins, nucle omorphs retain hundreds of genetic-housekeeping genes(5). Nucleomorph DNA r eplication and periplastid protein synthesis require the import of many nuc lear gene products across endoplasmic reticulum and periplastid membranes. The chromosomes have centromeres, but possibly only one loop domain, offeri ng a means for studying eukaryotic chromosome replication, segregation and evolution.