Complete Nucleomorph Genome Sequence of the Nonphotosynthetic Alga Cryptomonas paramecium Reveals a Core Nucleomorph Gene Set

Abstract

Nucleomorphs are the remnant nuclei of algal endosymbionts that were engulfed by nonphotosynthetic host eukaryotes. These peculiar organelles are found in cryptomonad and chlorarachniophyte algae, where they evolved from red and green algal endosymbionts, respectively. Despite their independent origins, cryptomonad and chlorarachniophyte nucleomorph genomes are similar in size and structure: they are both <1 million base pairs in size (the smallest nuclear genomes known), comprised three chromosomes, and possess subtelomeric ribosomal DNA operons. Here, we report the complete sequence of one of the smallest cryptomonad nucleomorph genomes known, that of the secondarily nonphotosynthetic cryptomonad Cryptomonas paramecium. The genome is 486 kbp in size and contains 518 predicted genes, 466 of which are protein coding. Although C. paramecium lacks photosynthetic ability, its nucleomorph genome still encodes 18 plastid-associated proteins. More than 90% of the “conserved” protein genes in C. paramecium (i.e., those with clear homologs in other eukaryotes) are also present in the nucleomorph genomes of the cryptomonads Guillardia theta and Hemiselmis andersenii. In contrast, 143 of 466 predicted C. paramecium proteins (30.7%) showed no obvious similarity to proteins encoded in any other genome, including G. theta and H. andersenii. Significantly, however, many of these “nucleomorph ORFans” are conserved in position and size between the three genomes, suggesting that they are in fact homologous to one another. Finally, our analyses reveal an unexpected degree of overlap in the genes present in the independently evolved chlorarachniophyte and cryptomonad nucleomorph genomes: ∼80% of a set of 120 conserved nucleomorph genes in the chlorarachniophyte Bigelowiella natans were also present in all three cryptomonad nucleomorph genomes. This result suggests that similar reductive processes have taken place in unrelated lineages of nucleomorph-containing algae.

Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs

“…Cryptophyte and chlorarachniophyte nucleomorphs are residual, endosymbiotic nuclei with tiny genomes ,1 Mb in size [14][15][16][17] Figure 1 | Cryptophyte and chlorarachniophyte cell biology. The cryptophyte alga G. theta and the chlorarachniophyte alga B. natans have plastids bound by four membranes.…”

“…Our results show that indirect 'solutions' have evolved, most notably the duplication and functional reassignment of host-derived nuclear genes. For example, a nucleusencoded cyclin-dependent kinase regulatory subunit protein (also known as kin(cdc)) predicted to function in the G. theta PPC or nucleomorph is not specifically related to kin(cdc) homologues encoded in the nucleomorph genomes of two other cryptophytes 14,16 , but instead is a recent duplicate of an apparently host-derived homologue ( Supplementary Fig. 2.5.2.2a).…”

Origin of eukaryotic cells: 40 years on

“…Nucleomorphs are now known to be remnant algal nuclei with a much-reduced coding capacity (Archibald 2007;Moore and Archibald 2009). Analyses of the genes that remain demonstrate beyond all doubt that the cryptophyte nucleomorph (and plastid) is of red algal origin (Douglas and Penny 1999;Douglas et al 2001;Lane et al 2007;Tanifuji et al 2011) while the nucleomorph of chlorarachniophytes is derived from a green algal endosymbiont (Gilson et al 2006;Rogers et al 2007).…”

Genomic perspectives on the birth and spread of plastids

“…In most complex algae the second wave of EGT has gone to completion: all essential genes for the maintenance of the plastid now reside in the secondary nucleus, and their protein products are imported to the organelle in a stepwise fashion as described above. Sequenced nucleomorph genomes from cryptophytes and chlorarachniophytes are all <1-Mb pairs in size and possess at most ∼500 genes and ∼30 genes for plastid-targeted proteins (44,(75)(76)(77)(78)(79). Consequently, the cyanobacterial footprint in the host nuclear genomes of complex algae should be roughly similar to that found in primary plastid-bearing algae, assuming their plastid proteomes are similarly sized (i.e., comprised of 1,000 or more proteins; see below).…”