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. 2013 Sep;7(9):1764-74.
doi: 10.1038/ismej.2013.70. Epub 2013 May 2.

Gene invasion in distant eukaryotic lineages: discovery of mutually exclusive genetic elements reveals marine biodiversity

Adam Monier  1 , Sebastian Sudek, Naomi M Fast, Alexandra Z Worden
Affiliations

Gene invasion in distant eukaryotic lineages: discovery of mutually exclusive genetic elements reveals marine biodiversity

Adam Monier et al. ISME J. 2013 Sep.

Abstract

Inteins are rare, translated genetic parasites mainly found in bacteria and archaea, while spliceosomal introns are distinctly eukaryotic features abundant in most nuclear genomes. Using targeted metagenomics, we discovered an intein in an Atlantic population of the photosynthetic eukaryote, Bathycoccus, harbored by the essential spliceosomal protein PRP8 (processing factor 8 protein). Although previously thought exclusive to fungi, we also identified PRP8 inteins in parasitic (Capsaspora) and predatory (Salpingoeca) protists. Most new PRP8 inteins were at novel insertion sites that, surprisingly, were not in the most conserved regions of the gene. Evolutionarily, Dikarya fungal inteins at PRP8 insertion site a appeared more related to the Bathycoccus intein at a unique insertion site, than to other fungal and opisthokont inteins. Strikingly, independent analyses of Pacific and Atlantic samples revealed an intron at the same codon as the Bathycoccus PRP8 intein. The two elements are mutually exclusive and neither was found in cultured Bathycoccus or other picoprasinophyte genomes. Thus, wild Bathycoccus contain one of few non-fungal eukaryotic inteins known and a rare polymorphic intron. Our data indicate at least two Bathycoccus ecotypes exist, associated respectively with oceanic or mesotrophic environments. We hypothesize that intein propagation is facilitated by marine viruses; and, while intron gain is still poorly understood, presence of a spliceosomal intron where a locus lacks an intein raises the possibility of new, intein-primed mechanisms for intron gain. The discovery of nucleus-encoded inteins and associated sequence polymorphisms in uncultivated marine eukaryotes highlights their diversity and reveals potential sexual boundaries between populations indistinguishable by common marker genes.

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Figures

Figure 1
Figure 1
Maximum-likelihood phylogenetic analysis of PRP8 protein sequences using 1921 extein positions. Stars denote groups with previously known (black) intein-containing members and those identified herein (fuchsia). Stramenopiles, Alveolates and Rhizaria are abbreviated as SAR. The scale bar reflects substitutions per site. Bootstrap support ⩾75% is shown.
Figure 2
Figure 2
Intein domain architecture. (a) Schematic of extein, conserved intein-splicing motif (blocks A, B, F and G), and homing endonuclease (blocks C, D, E and H) domains. (b) Alignment of PRP8 intein splicing and HE motifs from the wild Bathycoccus targeted metagenome, environmental clone TAfiPRP8 (from unsorted Tropical Atlantic DNA) and fungal representatives from different insertion sites. Essential (asterisks) and non-essential (dots) splice junction residues and HE catalytic (asterisks) and other essential (square; lysine, K) residues are indicated. Residue ‘X' in TAfiPRP8 block D represents an ambiguous base call resulting in possible codons AAG or CAG (residue K or Q). Conserved residues are colored according to physicochemical properties (ClustalX color scheme). Histogram shows overall conservation levels; amino acids located between bracketed blocks were omitted.
Figure 3
Figure 3
Intein insertion sites (dashed lines) along 2309 residues of PRP8 and the corresponding amino-acid conservation profile for taxa from different eukaryotic supergroups (as in Figure 1). Higher Y-axis values indicate lower conservation at that position (that is, a greater number of different amino acids). Dots show exact insertion sites and newly identified sites are in black frames.
Figure 4
Figure 4
PRP8 polymorphic intervening sequences in Bathycoccus. (a) Schematic of Bathycoccus intervening and insert-less sequence types. (b) Geographic locations of polymorphic Bathycoccus PRP8 sequences. (c) Phylogenetic relationships among PRP8 coding sequences (nucleotides) that flank intein insertion site d of wild Bathycoccus. Phylogenetic grouping is driven by variations at the third-codon position and this tree should not be used for evolutionary distances as these positions may be saturated. Node support ⩾75% is shown (black dots).
Figure 5
Figure 5
Phylogenetic relationships among intein splicing motifs from Bathycoccus (both metagenomic and PCR-based), the choanoflagellate S. rosetta, fungi, and the nearest outside group (inteins from bacterial and viral genes) are shown in this subtree derived from an analysis of 453 inteins (Supplementary Figure 5). Approximate maximum-likelihood inference was used on 51 amino-acid positions, representing conserved blocks A, B, F and G. NEB InBase identifiers precede species names. Node support is indicated where ⩾75% and substitutions per site (scale bar) are shown. PRP8 inteins are at site a unless noted otherwise.
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