Short-term sequence evolution and vertical inheritance of the Naegleria twin-ribozyme group I intron

Odd-Gunnar Wikmark,Johan F De Jonckheere,Steinar D Johansen,Christer Einvik

doi:10.1186/1471-2148-6-39

Abstract

BackgroundRibosomal DNA of several species of the free-living Naegleria amoeba harbors an optional group I intron within the nuclear small subunit ribosomal RNA gene. The intron (Nae.S516) has a complex organization of two ribozyme domains (NaGIR1 and NaGIR2) and a homing endonuclease gene (NaHEG). NaGIR2 is responsible for intron excision, exon ligation, and full-length intron RNA circularization, reactions typical for nuclear group I intron ribozymes. NaGIR1, however, is essential for NaHEG expression by generating the 5' end of the homing endonuclease messenger RNA. Interestingly, this unusual class of ribozyme adds a lariat-cap at the mRNA.ResultsTo elucidate the evolutionary history of the Nae.S516 twin-ribozyme introns we have analyzed 13 natural variants present in distinct Naegleria isolates. Structural variabilities were noted within both the ribozyme domains and provide strong comparative support to the intron secondary structure. One of the introns, present in N. martinezi NG872, contains hallmarks of a degenerated NaHEG. Phylogenetic analyses performed on separate data sets representing NaGIR1, NaGIR2, NaHEG, and ITS1-5.8S-ITS2 ribosomal DNA are consistent with an overall vertical inheritance pattern of the intron within the Naegleria genus.ConclusionThe Nae.S516 twin-ribozyme intron was gained early in the Naegleria evolution with subsequent vertical inheritance. The intron was lost in the majority of isolates (70%), leaving a widespread but scattered distribution pattern. Why the apparent asexual Naegleria amoebae harbors active intron homing endonucleases, dependent on sexual reproduction for its function, remains a puzzle.

Highlights

Ribosomal DNA of several species of the free-living Naegleria amoeba harbors an optional group I intron within the nuclear small subunit ribosomal RNA gene
Introns have been noted at position 516 in small subunit (SSU) ribosomal DNA (rDNA) and at positions 1921, 1926, 1949, and 2563 in large subunit (LSU) rDNA [5,6,7,8,9,10,11]
Group I introns at position 516 in SSU rDNA are relatively common among eukaryotic microorganisms with more than 250 cases reported so far [16,17], and with both lateral and vertical inheritance patterns compared to that of host rDNA

Summary

Introduction

Ribosomal DNA of several species of the free-living Naegleria amoeba harbors an optional group I intron within the nuclear small subunit ribosomal RNA gene. The intron (Nae.S516) has a complex organization of two ribozyme domains (NaGIR1 and NaGIR2) and a homing endonuclease gene (NaHEG). NaGIR1, is essential for NaHEG expression by generating the 5' end of the homing endonuclease messenger RNA. This unusual class of ribozyme adds a lariat-cap at the mRNA. A typical Naegleria amoeba cell contains a distinct (page number not for citation purposes). Some Naegleria isolates have been reported to contain group I intron insertions at conserved sequence sites, both within the small subunit (SSU) and large subunit (LSU) rRNA genes [5]. Introns have been noted at position 516 in SSU rDNA (i.e. a position that is homologous to corresponding position in the E. coli rRNA gene) and at positions 1921, 1926, 1949, and 2563 in LSU rDNA [5,6,7,8,9,10,11]

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