Barriers to Intron Promiscuity in Bacteria

Abstract

2"The field of bacterial viruses is a fine playground for serious children who ask ambitious questions."Max DelbruckThe first bacterial intron, a self-splicing group I intron, was found to interrupt the thymidylate synthase (td) gene of the Escherichia coli phage T4 (11). The second and third bacterial group I introns were found to interrupt the aerobic (nrdB) and anaerobic (nrdD [initially named sunY]) ribonucleotide reductases of phage T4 (29,90), and another group I intron was soon discovered in the DNA polymerase gene of SPO1, a Bacillus phage (25). From this (admittedly) small sampling of phage genomes, one might have naively expected that group I introns would be abundant in phage or bacterial genomes, especially since subsequent laboratory experiments demonstrated that group I introns could propagate themselves (by a process called homing) throughout populations of intron-minus alleles with near 100% efficiency (5, 68). That a similar homing phenomenon had also been previously demonstrated for a group I intron in the large rRNA gene of yeast mitochondria (34) gave additional support to the notion that group I introns should be able to spread efficiently throughout populations. However, this expected outcome has never been realized in natural phage populations; some phage populations harbor many introns, while other related phage populations are strangely lacking in any introns whatsoever (Table 1). Why do group I introns have an unusual distribution in phage and bacterial genomes, and what potential barriers might exist to prevent their spread?A similar question might be asked of group II introns in bacteria. Much was made of the initial finding of group II introns in bacteria, as their discovery added fuel to the debate concerning the evolutionary origins of eukaryotic spliceosomal introns (22, 70) which have both structural and functional similarities to group II introns (53,79,84). Yet, the number of group II introns in bacteria is small, many of which are inferred only from database matches to reverse transcriptases or maturases encoded within known introns (13,41,73,89), and only two have been shown to splice or be mobile in vivo (48,49,55,80) (Table 2). While group II intron homing is mechanistically distinct from group I intron homing, the principle is similar; group II introns home from intron-containing to intronless alleles. Many elegant biochemical and genetic experiments have unraveled the complexities of bacterial group II intron homing (14,48,49), and based on these results, there seems no a priori reason why group II introns should not be able to spread efficiently through populations of intron-minus alleles. The paucity of bacterial group II introns becomes even more perplexing given the recent demonstration of group II intron transposition to novel chromosomal sites (15). That group II introns are abundant in mitochondrial and chloroplast genomes (52) and present in bacterial genomes but at lower levels (and absent in phages) only adds to the mystery surrounding the lack of group II intro...

Multiple self-splicing introns in the 16S rRNA genes of giant sulfur bacteria

“…Introns have been well studied regarding their splicing mechanism from RNA precursors and their methods of propagation in the host genome (35,46,(53)(54)(55)(56)(57). Here we show that introns in large sulfur bacteria also demonstrate self-splicing abilities in vitro (Fig.…”

Form species Nostoc commune (Cyanobacteria).

“…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). Recent work also suggests that the evolution of the intron in the tRNA Leu (UAA) gene is considerably more complex than previously thought (Rudi & Jakobsen, 1999).…”

“…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.…”

“…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).…”

Insertion of a homing endonuclease creates a genes-in-pieces ribonucleotide reductase that retains function

“…Many characterized homing endonucleases have recognition sites that lie in genes that function in DNA metabolism, including those that encode aerobic and anaerobic ribonucleotide reductases (RNRs) (13). Three classes of RNRs have been described to date, based on required metallocofactors used to generate a radical intermediate and on structural differences (14).…”