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Nucleomorph genome of Hemiselmis andersenii reveals complete intron loss and compaction as a driver of protein structure and function.

ABSTRACT: Nucleomorphs are the remnant nuclei of algal endosymbionts that took up residence inside a nonphotosynthetic eukaryotic host. The nucleomorphs of cryptophytes and chlorarachniophytes are derived from red and green algal endosymbionts, respectively, and represent a stunning example of convergent evolution: their genomes have independently been reduced and compacted to <1 megabase pairs (Mbp) in size (the smallest nuclear genomes known) and to a similar three-chromosome architecture. The molecular processes underlying genome reduction and compaction in eukaryotes are largely unknown, as is the impact of reduction/compaction on protein structure and function. Here, we present the complete 0.572-Mbp nucleomorph genome of the cryptophyte Hemiselmis andersenii and show that it is completely devoid of spliceosomal introns and genes for splicing RNAs-a case of complete intron loss in a nuclear genome. Comparison of H. andersenii proteins to those encoded in the slightly smaller (0.551-Mbp) nucleomorph genome of another cryptophyte, Guillardia theta, and to their homologs in the unicellular red alga Cyanidioschyzon merolae reveal that (i) cryptophyte nucleomorph genomes encode proteins that are significantly smaller than those in their free-living algal ancestors, and (ii) the smaller, more compact G. theta nucleomorph genome encodes significantly smaller proteins than that of H. andersenii. These results indicate that genome compaction can eliminate both coding and noncoding DNA and, consequently, drive the evolution of protein structure and function. Nucleomorph proteins have the potential to reveal the minimal functional units required for basic eukaryotic cellular processes.

SUBMITTER: Lane CE

PROVIDER: S-EPMC2148396 | biostudies-literature | 2007 Dec

REPOSITORIES: biostudies-literature

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Nucleomorph genome of Hemiselmis andersenii reveals complete intron loss and compaction as a driver of protein structure and function.

Lane Christopher E CE van den Heuvel Krystal K Kozera Catherine C Curtis Bruce A BA Parsons Byron J BJ Bowman Sharen S Archibald John M JM

Proceedings of the National Academy of Sciences of the United States of America 20071206 50

Nucleomorphs are the remnant nuclei of algal endosymbionts that took up residence inside a nonphotosynthetic eukaryotic host. The nucleomorphs of cryptophytes and chlorarachniophytes are derived from red and green algal endosymbionts, respectively, and represent a stunning example of convergent evolution: their genomes have independently been reduced and compacted to <1 megabase pairs (Mbp) in size (the smallest nuclear genomes known) and to a similar three-chromosome architecture. The molecular ...[more]

PMID: 18077423

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Project description: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.

Dataset Information

Nucleomorph genome of Hemiselmis andersenii reveals complete intron loss and compaction as a driver of protein structure and function.

Publications

Nucleomorph genome of Hemiselmis andersenii reveals complete intron loss and compaction as a driver of protein structure and function.

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