Complete nucleotide sequence of the chlorarachniophyte nucleomorph: Nature’s smallest nucleus
- Paul R. Gilson*,†,
- Vanessa Su†,‡,
- Claudio H. Slamovits§,
- Michael E. Reith¶,
- Patrick J. Keeling§, and
- Geoffrey I. McFadden‡,‖
- *Infection and Immunity Division, The Walter and Eliza Hall Institute of Medical Research, Parkville 3050, Australia;
- ‡School of Botany, University of Melbourne, Victoria 3010, Australia;
- ¶Institute for Marine Biosciences, National Research Council, Halifax, NS, Canada B3H 3Z1; and
- §Department of Botany, University of British Columbia, Vancouver, BC, Canada V6T 1Z4
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Edited by Jeffrey D. Palmer, Indiana University, Bloomington, IN, and approved April 19, 2006
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↵ †P.R.G. and V.S. contributed equally to this work. (received for review January 26, 2006)
Abstract
The introduction of plastids into different heterotrophic protists created lineages of algae that diversified explosively, proliferated in marine and freshwater environments, and radically altered the biosphere. The origins of these secondary plastids are usually inferred from the presence of additional plastid membranes. However, two examples provide unique snapshots of secondary-endosymbiosis-in-action, because they retain a vestige of the endosymbiont nucleus known as the nucleomorph. These are chlorarachniophytes and cryptomonads, which acquired their plastids from a green and red alga respectively. To allow comparisons between them, we have sequenced the nucleomorph genome from the chlorarachniophyte Bigelowiella natans: at a mere 373,000 bp and with only 331 genes, the smallest nuclear genome known and a model for extreme reduction. The genome is eukaryotic in nature, with three linear chromosomes containing densely packed genes with numerous overlaps. The genome is replete with 852 introns, but these are the smallest introns known, being only 18, 19, 20, or 21 nt in length. These pygmy introns are shown to be miniaturized versions of normal-sized introns present in the endosymbiont at the time of capture. Seventeen nucleomorph genes encode proteins that function in the plastid. The other nucleomorph genes are housekeeping entities, presumably underpinning maintenance and expression of these plastid proteins. Chlorarachniophyte plastids are thus serviced by three different genomes (plastid, nucleomorph, and host nucleus) requiring remarkable coordination and targeting. Although originating by two independent endosymbioses, chlorarachniophyte and cryptomonad nucleomorph genomes have converged upon remarkably similar architectures but differ in many molecular details that reflect two distinct trajectories to hypercompaction and reduction.
Footnotes
- ‖To whom correspondence should be addressed. E-mail: gim{at}unimelb.edu.au
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Author contributions: P.R.G. and G.I.M. designed research; P.R.G., V.S., and C.H.S. performed research; P.R.G., V.S., M.E.R., and G.I.M. contributed new reagents/analytic tools; and P.R.G., V.S., C.H.S., M.E.R., P.J.K., and G.I.M. analyzed data.
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Conflict of interest statement: No conflicts declared.
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This paper was submitted directly (Track II) to the PNAS office.
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Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. DQ158856, DQ158857, and DQ158858).
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See Commentary on page 9379.
- © 2006 by The National Academy of Sciences of the USA
