A Phylogenetic Approach to Structural Variation in Organization of Nuclear Group I Introns and Their Ribozymes

Nuclear group I introns are restricted to the ribosomal DNA locus where they interrupt genes for small subunit and large subunit ribosomal RNAs at conserved sites in some eukaryotic microorganisms. Here, the myxomycete protists are a frequent source of nuclear group I introns due to their unique life strategy and a billion years of separate evolution. The ribosomal DNA of the myxomycete Mucilago crustacea was investigated and found to contain seven group I introns, including a direct repeat-containing intron at insertion site S1389 in the small subunit ribosomal RNA gene. We collected, analyzed, and compared 72 S1389 group IC1 introns representing diverse myxomycete taxa. The consensus secondary structure revealed a conserved ribozyme core, but with surprising sequence variations in the guanosine binding site in segment P7. Some S1389 introns harbored large extension sequences in the peripheral region of segment P9 containing direct repeat arrays. These repeats contained up to 52 copies of a putative internal guide sequence motif. Other S1389 introns harbored homing endonuclease genes in segment P1 encoding His-Cys proteins. Homing endonuclease genes were further interrupted by small spliceosomal introns that have to be removed in order to generate the open reading frames. Phylogenetic analyses of S1389 intron and host gene indicated both vertical and horizontal intron transfer during evolution, and revealed sporadic appearances of direct repeats, homing endonuclease genes, and guanosine binding site variants among the myxomycete taxa.

Automated summary

Nuclear group I introns are mainly found in the ribosomal DNA locus of some eukaryotic microorganisms, with myxomycete protists being a significant source due to their unique evolutionary history and life strategies. Analysis of S1389 group IC1 introns in diverse myxomycete taxa revealed a conserved ribozyme core structure with variations in guanosine binding sites and extension sequences, as well as the presence of homing endonuclease genes and direct repeat arrays. Phylogenetic analyses suggested both vertical and horizontal intron transfer during evolution in myxomycetes.