Nucleomorph Genome Sequence of the Cryptophyte Alga Chroomonas mesostigmatica CCMP1168 Reveals Lineage-Specific Gene Loss and Genome Complexity

Abstract

Cryptophytes are a diverse lineage of marine and freshwater, photosynthetic and secondarily nonphotosynthetic algae that acquired their plastids (chloroplasts) by “secondary” (i.e., eukaryote–eukaryote) endosymbiosis. Consequently, they are among the most genetically complex cells known and have four genomes: a mitochondrial, plastid, “master” nuclear, and residual nuclear genome of secondary endosymbiotic origin, the so-called “nucleomorph” genome. Sequenced nucleomorph genomes are ∼1,000-kilobase pairs (Kbp) or less in size and are comprised of three linear, compositionally biased chromosomes. Although most functionally annotated nucleomorph genes encode proteins involved in core eukaryotic processes, up to 40% of the genes in these genomes remain unidentifiable. To gain insight into the function and evolutionary fate of nucleomorph genomes, we used 454 and Illumina technologies to completely sequence the nucleomorph genome of the cryptophyte Chroomonas mesostigmatica CCMP1168. At 702.9 Kbp in size, the C. mesostigmatica nucleomorph genome is the largest and the most complex nucleomorph genome sequenced to date. Our comparative analyses reveal the existence of a highly conserved core set of genes required for maintenance of the cryptophyte nucleomorph and plastid, as well as examples of lineage-specific gene loss resulting in differential loss of typical eukaryotic functions, e.g., proteasome-mediated protein degradation, in the four cryptophyte lineages examined.

Nucleomorph and plastid genome sequences of the chlorarachniophyte Lotharella oceanica: convergent reductive evolution and frequent recombination in nucleomorph-bearing algae

“…Repetitive sequences were found in the nucleomorph genome of the cryptophyte C. mesostigmatica [21], but in that case they consisted of A-T-rich simple repeats such as [TTA] n located in the ITS between the 5S and 28S rDNA, and [AT 4–5 ] 14 and [TA 2 GA 2 TA 5 ] 4–25 in intergenic spacers of the sub-telomeric repeats. A long homopolymer of [A/T] 24–37 was also found in several sites within 28S rDNA in C. mesostigmatica .…”

Protein import into complex plastids: Cellular organization of higher complexity

“…However, in respect to "chromalveolates", the PPC of the cryptophytes, harbors an additional and therefore second cell nucleus called nucleomorph (Gillot and Gibbs, 1980;Maier et al, 2000a) A c c e p t e d M a n u s c r i p t It is a dwarf version of the nucleus of the secondary eukaryotic endosymbiont, and represents, with less than 1000 kb, one of nature's smallest cell nuclei. An early genome project on one of the nucleomorph genomes highlighted a very compact genome (Douglas et al, 2001), which was later also seen in other cryptophytic nucleomorphs (Lane et al, 2007;Moore et al, 2012;Tanifuji et al, 2011). By rescanning the nucleomorph sequence, some homologs to components of an ERAD (ER-associated degradation)-system were detected several years after publishing the first nucleomorph genome .…”

Polyploidy of Endosymbiotically Derived Genomes in Complex Algae

“…Many syntenic regions with the same gene order among different species were found in cryptophyte nucleomorph genomes (Lane et al 2007; Tanifuji et al 2011; Moore et al 2012), as well as draft genomes of chlorarachniophyte nucleomorphs. Overlapping gene transcription has also been reported in nucleomorph genomes (Williams et al 2005).…”