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Published online on December 6, 2007, 10.1073/pnas.0707419104

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

Christopher E. Lane*, Krystal van den Heuvel*, Catherine Kozera{dagger}, Bruce A. Curtis{dagger}, Byron J. Parsons{dagger},{ddagger}, Sharen Bowman{dagger},§, and John M. Archibald*

*Canadian Institute for Advanced Research, Integrated Microbial Biodiversity Program, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS, Canada B3H 1X5; §Department of Process Engineering and Applied Science, Dalhousie University, Halifax, NS, Canada B3H 3J5; and {dagger}Atlantic Genome Centre, Halifax, NS, Canada B3J 1S5

Edited by Jeffrey D. Palmer, Indiana University, Bloomington, IN, and approved October 29, 2007 (received for review August 6, 2007)

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.

endosymbiosis | genome evolution | genome reduction


Footnotes

Author contributions: J.M.A. designed research; C.E.L., K.v.d.H., C.K., B.A.C., B.J.P., and S.B. performed research; C.K., B.A.C., B.J.P., and S.B. contributed new reagents/analytic tools; C.E.L., K.v.d.H., B.A.C., and J.M.A. analyzed data; and C.E.L. and J.M.A. wrote the paper.

{ddagger}Present address: Ocean Nutrition Canada, 101 Research Drive, Dartmouth, NS, Canada B2Y 4T6.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

To whom correspondence should be addressed. E-mail: john.archibald{at}dal.ca


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