Complete nucleotide sequence of the chlorarachniophyte nucleomorph: nature's smallest nucleus - PubMed (original) (raw)

Complete nucleotide sequence of the chlorarachniophyte nucleomorph: nature's smallest nucleus

Paul R Gilson et al. Proc Natl Acad Sci U S A. 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.

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Conflict of interest statement

Conflict of interest statement: No conflicts declared.

Figures

Fig. 1.

Fig. 1.

Evolution of chlorarachniophytes such as B. natans by sequential endosymbioses. Enslavement of a photosynthetic, cyanobacterium-like prokaryote (Cb) introduces photosynthesis into a eukaryotic host (Euk 1), whose nucleus (Nu1) acquires at least 1,000 cyanobacterial genes over time. Secondary endosymbiosis involves capture and retention of the primary photosynthetic eukaryote by another eukaryote (Euk 2), producing a plastid with four bounding membranes such as those of cryptomonads, chlorarachniophytes, haptophyte and heterokont algae, and malaria parasites. Essential plastid protein genes are transferred from the endosymbiont nucleus (Nm, nucleomorph) to the nucleus (Nu2) of the second eukaryotic host. Here, we show that only 17 of the original plastid protein genes remain in the nucleomorph of B. natans, preventing its loss.

Fig. 2.

Fig. 2.

Gene map of the three B. natans nucleomorph chromosomes. Inverted terminal repeats are shaded in yellow. Pygmy introns are depicted as triangles. Genes for which excision of the pygmy introns (where present) has been confirmed by cDNA analysis are named in red type.

Fig. 3.

Fig. 3.

Nucleomorph genes harbor numerous ultra-small introns. (A) Consensus plots of the 18-, 19-, 20- and 21-nt introns showing 5′-GT. . .AG-3′ borders but no exon or intron core consensus other than an A at −2. This A and overall high AT content are the only discernible differences between real introns and 19-nt exonic sequences with 5′-GT. . .AG-3′ borders (pseudointrons) that are not removed by the spliceosome. (B) Nineteen nucleotide introns are the most abundant in the nucleomorph, but equivalent numbers of each size category of pseudointrons occur. (C) Numbers of introns shared between the nucleomorph, Arabidopsis, and Chlamydomonas. Most nucleomorph introns occur at the same position as large introns in these closely related genomes, suggesting that the pygmy introns began as normal introns but have been reduced by DNA loss to converge on a minimal spliceable size, ≈19 nt.

Fig. 4.

Fig. 4.

Comparison of gene functional categories from the nucleomorph genomes of B. natans and G. theta. Percentages of genes belonging to different functional categories are indicated by the scale bar on the left, and the total numbers of genes belonging to these categories are shown above the class bars.

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