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

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.

Diversity of Viruses Infecting the Green Microalga Ostreococcus lucimarinus

“…employed under nonoptimal conditions. No inteins were identified in these viral genomes, although inteins with homing endonucleases have been observed in prasinoviruses (62), including some Ostreococcus viruses (63), and in some green algae, including Bathycoccus, with viruses being a proposed mechanism for propagation (64).…”

Abundance and Biogeography of Picoprasinophyte Ecotypes and Other Phytoplankton in the Eastern North Pacific Ocean

“…The Bathycoccus genus is thought to consist of a single species (Bathycoccus prasinos), and only one cultured strain (Bban7, also known as RCC1105) has a sequenced genome (15). Cultured Bathycoccus strains and environmental clones have 100% 18S rRNA gene identity, unlike the Micromonas and Ostreococcus clades (16)(17)(18). However, targeted metagenomic data from the tropical Atlantic suggest that different Bathycoccus ecotypes may exist, based largely on an intron/intein presence/absence polymorphism in the gene PRP8 (18,19).…”

“…Cultured Bathycoccus strains and environmental clones have 100% 18S rRNA gene identity, unlike the Micromonas and Ostreococcus clades (16)(17)(18). However, targeted metagenomic data from the tropical Atlantic suggest that different Bathycoccus ecotypes may exist, based largely on an intron/intein presence/absence polymorphism in the gene PRP8 (18,19). Notably, the internal transcribed spacer (ITS) from the tropical Atlantic wild Bathycoccus metagenome also branches separately from cultured strains (18), while the ITS from cultured strains and two coastal Chilean Bathycoccus metagenomes are similar (20).…”

“…However, targeted metagenomic data from the tropical Atlantic suggest that different Bathycoccus ecotypes may exist, based largely on an intron/intein presence/absence polymorphism in the gene PRP8 (18,19). Notably, the internal transcribed spacer (ITS) from the tropical Atlantic wild Bathycoccus metagenome also branches separately from cultured strains (18), while the ITS from cultured strains and two coastal Chilean Bathycoccus metagenomes are similar (20). Sequence variations have led to the proposal that two (18) or more (20) ecotypes exist and that the ecotypes may partition between mesotrophic and oligotrophic environments (18).…”

“…Notably, the internal transcribed spacer (ITS) from the tropical Atlantic wild Bathycoccus metagenome also branches separately from cultured strains (18), while the ITS from cultured strains and two coastal Chilean Bathycoccus metagenomes are similar (20). Sequence variations have led to the proposal that two (18) or more (20) ecotypes exist and that the ecotypes may partition between mesotrophic and oligotrophic environments (18). However, little is known about overall genetic distances and whether the observed sequence variants do indeed correspond to ecotype-level differences.…”