Complete nucleotide sequence of the chlorarachniophyte nucleomorph: Nature’s smallest nucleus

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 secondaryendosymbiosis-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.plastid ͉ secondary endosymbiosis ͉ intron ͉ endosymbiosis T he origin of plastids through endosymbiosis of a cyanobacterium-like prokaryote transferred photosynthesis into eukaryotes and launched a massive wave of diversification that subsequently generated a tremendous range of algae and plants (1). This initial event is referred to as primary endosymbiosis ( Fig. 1) and created a plastid with two membranes such as those of green algae, plants, red algae, and glaucophyte algae (1). Transfer of genes from the endosymbiont to the nuclear genome of the host initially led to dependence of the endosymbiont on the host that was necessary to stabilize the partnership (2). Ongoing transfer has resulted in reduction of the prokaryotic genome, so that plastid DNA now represents probably Ͻ10% of its original gene content, and increasingly sophisticated regulation of the endosymbiont by the host has resulted in endosymbiont replication, gene expression, metabolic activity, and even death being managed by the eukaryotic host (3). Indeed, primary plastids seem to retain some autonomy only in the synthesis and deployment of redox proteins involved in photosynthetic electron transfer (4).A...

Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs

“…In contrast, B. natans has a larger number of predicted nucleomorph-localized, spliceosome-associated proteins than does G. theta (Supplementary Fig. 2.4.1), which correlates with the marked difference in intron abundance: 852 in the B. natans nucleomorph genome 15 versus just 17 in G. theta 17 ).…”

“…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.…”

“…Indeed, why nucleomorph genomes have been retained at all is a long-standing mystery of plastid evolution. Bearing in mind our knowledge of the G. theta and B. natans plastid 22,23 , nucleomorph 15,17 and mitochondrial (this study) genome sequences, we carried out a comprehensive examination of nucleus-encoded proteins predicted to be targeted to each subcellular compartment (Supplementary Information 1.9), with emphasis on the PPC.…”

Babesia microti-Group Parasites Compared Phylogenetically by Complete Sequencing of the CCT.ETA. Gene in 36 Isolates

“…Other than in piroplasmids, such tiny introns have not been demonstrated in the CCTη gene from alveolates such as the apicomplexans Toxoplasma, Neospora, and Plasmodium and the ciliate Tetrahymena. Comparatively small (25 to 29 nt) introns reside in the CCTη gene of ciliate Paramecium (GenBank accession number NC_006058), and the tiny introns (~19 to 23 nt) have been reported in macronuclear genome of Paramecium [29] and nucleomorph genome of chlorarachniophytes [7]. Gilson et al surmised that the tiny introns in chlorarachniophytes may originate as miniaturizations of the larger introns present in the endosymbiont at the time of capture [7].…”

Advances in genetic engineering of marine algae

“…The plastid genomes vary broadly in size and gene content (Green, 2011, Grzebyk et al, 2003, and for several peridinin-containing dinoflagellates, the plastid genomes have substantially decreased to one or two genes or even none at all (Zhang et al, 1999). Cryptomonads (containing a red algal plastid) and Chlorarachniophytes (green algal plastid) coordinate four genomes (two nuclear and one each from the plastid or the mitochondria) (Gilson et al, 2006, Tanifuji et al, 2011. In the remnant nucleomorph genome of Cryptomonad Guillardia theta, half of the genes code for unknown function proteins (Douglas et al, 2001).…”