Survey of group I and group II introns in 29 sequenced genomes of the Bacillus cereus group: insights into their spread and evolution

Tourasse, Nicolas J.; Kolstø, Anne‐Brit

doi:10.1093/nar/gkn372

Cited by 54 publications

(63 citation statements)

References 88 publications

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“…Phylogenetic analysis of the most frequently observed intron S1396, a group II intron, revealed that it was probably acquired both vertically and horizontally within the family. This feature is well known among group II introns (46)(47)(48)(49). Comparative sequence analysis of intron S1396 generally reflects the phylogeny suggested by 16S rRNA sequence analysis at species level (Table S1 and Fig.…”

Section: Discussionsupporting

confidence: 72%

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

Salman

Amann

Shub³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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The gene encoding the small subunit rRNA serves as a prominent tool for the phylogenetic analysis and classification of Bacteria and Archaea owing to its high degree of conservation and its fundamental function in living organisms. Here we show that the 16S rRNA genes of not-yet-cultivated large sulfur bacteria, among them the largest known bacterium Thiomargarita namibiensis , regularly contain numerous self-splicing introns of variable length. The 16S rRNA genes can thus be enlarged to up to 3.5 kb. Remarkably, introns have never been identified in bacterial 16S rRNA genes before, although they are the most frequently sequenced genes today. This may be caused in part by a bias during the PCR amplification step that discriminates against longer homologs, as we show experimentally. Such length heterogeneity of 16S rRNA genes has so far never been considered when constructing 16S rRNA-based clone libraries, even though an elongation of rRNA genes due to intervening sequences has been reported previously. The detection of elongated 16S rRNA genes has profound implications for common methods in molecular ecology and may cause systematic biases in several techniques. In this study, catalyzed reporter deposition–fluorescence in situ hybridization on both ribosomes and rRNA precursor molecules as well as in vitro splicing experiments were performed and confirmed self-splicing of the introns. Accordingly, the introns do not inhibit the formation of functional ribosomes.

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Section: Discussionsupporting

confidence: 72%

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

Salman

Amann

Shub³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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“…In bacteria, group I and group II introns are small mobile elements (0.2 to 1 kb and 0.7 to 3 kb, respectively) that are transcribed into self-splicing RNAs (147,148). These introns are widespread within the bacterial kingdom but not very abundant.…”

Section: Inteins Introns and Retroelementsmentioning

confidence: 99%

Bacterial Genome Instability

Darmon

Leach

2014

Microbiol Mol Biol Rev

336

289

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SUMMARY Bacterial genomes are remarkably stable from one generation to the next but are plastic on an evolutionary time scale, substantially shaped by horizontal gene transfer, genome rearrangement, and the activities of mobile DNA elements. This implies the existence of a delicate balance between the maintenance of genome stability and the tolerance of genome instability. In this review, we describe the specialized genetic elements and the endogenous processes that contribute to genome instability. We then discuss the consequences of genome instability at the physiological level, where cells have harnessed instability to mediate phase and antigenic variation, and at the evolutionary level, where horizontal gene transfer has played an important role. Indeed, this ability to share DNA sequences has played a major part in the evolution of life on Earth. The evolutionary plasticity of bacterial genomes, coupled with the vast numbers of bacteria on the planet, substantially limits our ability to control disease.

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“…By contrast, bacteriophages have a global gene pool with intense horizontal exchange occurring among genetically related local groups of phages and low-grade exchange of sequences occurring over wide phylogenetic distances (34), making them ideal vehicles for the transfer of HEs, introns, and inteins between phages, among bacteria, and between phages and bacteria. Further, in lysogeny the prophage provides a silent locus from which HEs can invade homologous host genes in bacteria (108). Introns and inteins also tend to target conserved genes that have both phage and bacterial copies, making insertions less toxic and improving the odds of homologous recombination (59,77).…”

Section: Disparate Origins Convergent Parasitic Strategiesmentioning

confidence: 99%

“…Increasingly, they are being found in a variety of protein-coding genes, including those for recombinase A and ribonucleotide reductase (77,108). In bacteriophages, they are seen both in tRNA genes and in some proteincoding genes, like those for DNA polymerase, ribonucleotide reductase, and thymidylate synthase (45).…”

Section: Group I Intronsmentioning

confidence: 99%

Group I Introns and Inteins: Disparate Origins but Convergent Parasitic Strategies

Raghavan

Minnick

2009

J Bacteriol

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Genomes of most organisms harbor DNA of foreign origin that has no known function. Since these elements may not contribute to a host's fitness but utilize host resources for their perpetuation, it is appropriate to consider them genetic parasites (4). With the advent of sequencing technologies, a wide variety of parasitic elements have been discovered in bacteria from all environments, including obligate intracellular pathogens (100), which were thought to be shielded from horizontal gene transfer (HGT). Detection of a parasitic genetic element in a genome represents only a snapshot of the continuing and dynamic interplay between the host's attempts to purge the element and the element's ability to persist. These adaptable genetic parasites have evolved mechanisms to overcome defenses (75) of the cellular machinery to ultimately invade, colonize, and replicate within the host. Their success is very evident in the human genome, which consists mostly of such apparently superfluous DNA (65). Even compact bacterial genomes packed with functional genes contain mobile genetic elements (100), underscoring their universality in nature.A number of parasitic genetic elements are found in bacterial genomes, including transposons, insertion sequences, prophages, introns, inteins, and intervening sequences. While bacteria, especially pathogenic bacteria, are well studied, their parasitic genetic elements have not received as much attention. In the past few years, while studying the obligate intracellular pathogen Coxiella burnetii, we came to appreciate the intimate relationship between bacterial hosts and parasitic elements (92,93). In addition, interesting new studies have shed light on the evolutionary histories of group I introns, inteins, and homing endonucleases (HEs) (9, 109) and infused excitement into the field. This minireview, which focuses on the biology and evolution of group I introns and inteins found in bacteria, is an attempt to catalyze interest among bacteriologists in these fascinating genetic parasites. GROUP I INTRONSIntrons are noncoding, intragenic regions that are removed from precursor RNA to form the mature RNA by splicing the exons (coding regions that flank introns) together. They are much more common in eukaryotes than in bacteria (50). Introns are classified into four groups based on splicing mechanisms (47): group I, group II/group III, spliceosomal, and tRNA/archaeal introns. Spliceosomal introns are found in eukaryotes and utilize spliceosomes (large protein-RNA complexes) for splicing (70), whereas tRNA introns splice with the help of specialized enzymes (74). Group I and group II introns are able to self-splice-using different mechanisms-without the aid of any proteins and are thus referred to as ribozymes (104). A self-splicing group I intron from Tetrahymena thermophila was one of the first ribozymes to be described, in the early 1980s (61). Ribozymes are considered legacies of a primordial RNA world, where RNA possessed both informationencoding and catalytic properties, before the adven...

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Survey of group I and group II introns in 29 sequenced genomes of the Bacillus cereus group: insights into their spread and evolution

Cited by 54 publications

References 88 publications

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

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

Bacterial Genome Instability

Group I Introns and Inteins: Disparate Origins but Convergent Parasitic Strategies

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