Origin and evolution of group I introns in cyanobacterial tRNA genes

Abstract

Many tRNA UAALeu genes from plastids contain a group I intron. An intron is also inserted in the same gene at the same position in cyanobacteria, the bacterial progenitors of plastids, suggesting an ancient bacterial origin for this intron. A group I intron has also been found in the tRNA fMet gene of some cyanobacteria but not in plastids, suggesting a more recent origin for this intron. In this study, we investigate the phylogenetic distributions of the two introns among cyanobacteria, from the earliest branching to the more derived species. The phylogenetic distribution of the tRNA UAA Leu intron follows the clustering of rRNA sequences, being either absent or present in clades of closely related species, with only one exception in the Pseudanabaena group. Our data support the notion that the tRNA UAA Leu intron was inherited by cyanobacteria and plastids through a common ancestor. Conversely, the tRNA fMet intron has a sporadic distribution, implying that many gains and losses occurred during cyanobacterial evolution. Interestingly, a phylogenetic tree inferred from intronic sequences clearly separates the different tRNA introns, suggesting that each family has its own evolutionary history.Ever since their discovery, the origin of introns has been a subject of controversy. One view, the introns-late hypothesis, proposes that introns are recent invaders and that split genes arose by late insertion of introns into originally uninterrupted genes (28). In that scenario, horizontal transfer and transposition of introns are frequent events, accounting for the scattered phylogenetic distribution of introns. Although the debate has focused on spliceosomal introns, such a scenario could apply as well to other types of introns, some of which are known to be mobile (22). In contrast, the introns-early view implies that introns are very ancient, being present in the progenote (universal ancestor) (7). The demonstration that some members of group I and group II introns are capable of in vitro autocatalytic activity (19,29,39) lends further support to the presence of these introns at an early stage of evolution, maybe as early as the putative precellular RNA world (13). In such a scenario, the observed phylogenetic distribution of introns could be explained by multiple losses in different lineages during evolution (7) and by their mobility, which is assumed to be a derived feature (2). A major obstacle for the introns-early hypothesis was the apparent absence of introns in eubacteria, although this was tentatively rationalized by pressure to streamline the genome in rapidly dividing bacteria (7). Discovery of group I introns in bacteriophages of gram-positive and gram-negative bacteria did not help to resolve the issue, due to uncertainties concerning the origin of the bacteriophages themselves (see discussion in reference 35). The recent discovery of both group I and group II introns in divergent eubacteria (4,11,12,20,31,44) was acclaimed as a breakthrough by introns-early proponents. In most cases, however, the relatio...

Form species Nostoc commune (Cyanobacteria).

“…Preliminary sequence analysis identified the products as amplified group I intron sequences with portions of the flanking tRNA Leu (UAA) exons. The position of insertion of the intron in the different tRNA Leu genes was, in each case, between U and A within the anticodon loop [conserved 5h-GGACUU 7 AA-3h ; the same position identified for other cyanobacterial group I introns in previous studies (Paquin et al, 1997)]. …”

“…Cyanobacterial populations have a number of advantages for such analyses : they have a cosmopolitan distribution ; they dominate the microbial populations of many extreme environments ; their colonies are often conspicuous and may assume macrophytic proportions ; colonies of what appear to be morphologically identical forms occur in geographically isolated environments ; growths, often attributed to a ' monospecific ' population, may cover many square kilometres ; and cyanobacteria have a D. Wright and others fossil record. Of those genetic markers that may resolve clusters and groupings within taxa below the level of genus, group I intron sequences have been investigated in a broad range of eubacterial taxa (Biniszkiewicz et al, 1994 ;Paquin et al, 1997Paquin et al, , 1999Edgell et al, 2000). In this study, we focussed on a large set of desiccated samples of free-living Nostoc for which detailed records were available of time and place of origin and taxonomic assignment.…”

“…Eubacterial group I introns were first identified in cyanobacteria (Kuhsel et al, 1990 ;Xu et al, 1990) ; their distribution within this group appears to be broad and includes a range of morphologically diverse forms including Microcystis, Scytonema, Gloeobacter and Nostoc (Paquin et al, 1997 ;Paulsrud & Lindblad, 1998 ;Rudi & Jakobsen, 1999). Group I introns interrupt protein-coding regions and RNA genes in eukaryotes and bacteriophages and are present in the anticodon loop of tRNA genes (Paquin et al, 1999) as well as in 23S rRNA in eubacteria (Everett et al, 1999).…”

“…There is controversy as to whether tRNA Leu (UAA) introns have an ancient or recent origin and whether they are stable or mobile (Besendahl et al, 2000 ;Edgell et al, 2000 ;Paquin et al, 1997Paquin et al, , 1999. In fact, current opinion is that there is no single reason that can adequately explain the current distribution of group I and group II introns in bacteria (Edgell et al, 2000).…”

The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification.

“…Unlike the majority of the other neomuran synapomorphies, there is no immediately obvious reason to regard splicing by proteins as an adaptation to thermophily or hot acid ; its occurrence in the neomuran ancestor might therefore have been purely fortuitous. Since group I selfsplicing introns occur in tRNA genes of cyanobacteria (Paquin et al, 1997 ;Besendahl et al, 2000), the probable sisters of posibacteria (see below), and occur in phage genes in posibacteria (Landthaler & Shub, 1999), they may already have been present in at least one tRNA gene of the neomuran ancestor. The substitution of a novel protein-splicing mechanism that recognized the secondary RNA structure of the splice junctions alone and no longer depended on that of the entire intron would immediately have allowed short duplications to occur in the anticodon loop without lethal consequences.…”