Abstract
The marine cyanobacterium Trichodesmium is unusual in its genomic architecture as 40% of the genome is occupied by non-coding DNA. Although the majority of it is transcribed into RNA, it is not well understood why such a large non-coding genome fraction is maintained. Mobile genetic elements can contribute to genome expansion. Many bacteria harbor introns whereas twintrons, introns-in-introns, are rare and not known to interrupt protein-coding genes in bacteria. Here we show the sequential in vivo splicing of a 5400 nt long group II twintron interrupting a highly conserved gene that is associated with RNase HI in some cyanobacteria, but free-standing in others, including Trichodesmium erythraeum. We show that twintron splicing results in a putatively functional mRNA. The full genetic arrangement was found conserved in two geospatially distinct metagenomic datasets supporting its functional relevance. We further show that splicing of the inner intron yields the free intron as a true circle. This reaction requires the spliced exon reopening (SER) reaction to provide a free 5′ exon. The fact that Trichodesmium harbors a functional twintron fits in well with the high intron load of these genomes, and suggests peculiarities in its genetic machinery permitting such arrangements.
Highlights
The diazotrophic Trichodesmium is a tropical marine cyanobacterium of global importance[1]
We found the host gene, which codes for a highly conserved cyanobacterial hypothetical protein, to be mis-annotated as RNase H, but instead to constitute a separate protein domain that is fused to RNase HI in several cyanobacteria
The host gene encodes a protein that is misannotated as RNase HI in some genomes, and as hypothetical protein in others
Summary
The diazotrophic Trichodesmium is a tropical marine cyanobacterium of global importance[1]. Group II introns constitute the largest class of prokaryotic introns They are frequently self-splicing, mobile ribozymes with conserved structural motifs and often possess an internal open reading frame (ORF) for an intron encoded protein (IEP). From the 17 group II introns in T. erythraeum documented to splice in vivo, ten lack an intron-located ORF3 These must either splice autocatalytically or depend on trans-encoded splicing factors. We found the host gene, which codes for a highly conserved cyanobacterial hypothetical protein, to be mis-annotated as RNase H, but instead to constitute a separate protein domain that is fused to RNase HI in several cyanobacteria Splicing of this twintron produces a putatively functional mRNA. We define the gene product of the mature mRNA as a novel protein domain that appears itself connected to RNA metabolism
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