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

Salman, Verena; Amann, Rudolf; Shub, David A.; Schulz-Vogt, Heide N.

doi:10.1073/pnas.1120192109

Cited by 67 publications

(62 citation statements)

References 78 publications

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“…S1 in the supplemental material), at least so far as 23S rRNA sequences are available to date, but it contains two intervening elements (Fig. 1A) similar to ones found in the rRNA genes of diverse species (e.g., see references [30][31][32], including other giant sulfur bacteria (33). In orange Guaymas Beggiatoa, a putative group I catalytic intron is found at E. coli position 1917, in the loop of predicted helix 69, and a putative LAGLIDADG homing endonuclease at E. coli position 1931, in a predicted unstructured region between helices 69 and 71 (Fig.…”

Section: Resultsmentioning

confidence: 99%

Mobile Elements in a Single-Filament Orange Guaymas Basin Beggiatoa (“Candidatus Maribeggiatoa”) sp. Draft Genome: Evidence for Genetic Exchange with Cyanobacteria

MacGregor

Biddle

Teske

2013

Appl Environ Microbiol

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The draft genome sequence of a single orange Beggiatoa ("Candidatus Maribeggiatoa") filament collected from a microbial mat at a hydrothermal site in Guaymas Basin (Gulf of California, Mexico) shows evidence of extensive genetic exchange with cyanobacteria, in particular for sensory and signal transduction genes. A putative homing endonuclease gene and group I intron within the 23S rRNA gene; several group II catalytic introns; GyrB and DnaE inteins, also encoding homing endonucleases; multiple copies of sequences similar to the fdxN excision elements XisH and XisI (required for heterocyst differentiation in some cyanobacteria); and multiple sequences related to an open reading frame (ORF) (00024_0693) of unknown function all have close non-Beggiatoaceae matches with cyanobacterial sequences. Sequences similar to the uncharacterized ORF and Xis elements are found in other Beggiatoaceae genomes, a variety of cyanobacteria, and a few phylogenetically dispersed pleiomorphic or filamentous bacteria. We speculate that elements shared among filamentous bacterial species may have been exchanged in microbial mats and that some of them may be involved in cell differentiation.

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Section: Resultsmentioning

confidence: 99%

Mobile Elements in a Single-Filament Orange Guaymas Basin Beggiatoa (“Candidatus Maribeggiatoa”) sp. Draft Genome: Evidence for Genetic Exchange with Cyanobacteria

MacGregor

Biddle

Teske

2013

Appl Environ Microbiol

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“…In keeping with the importance of a branched structure for retrotransposition, introns that lack a functional branchpoint do not encode a reverse transcriptase. Some of them, such as the trnV intron (Vogel and Börner 2002) which, like most other chloroplast introns, is strongly conserved in land plants, appear to have lost mobility altogether, while others belong to lineages that became associated with homing endonucleases (Toor and Zimmerly 2002;Mullineux et al 2010;Li et al 2011a;Salman et al 2012); the latter have long been known to ensure mobility of many group I and some archaeal introns by a mechanism in which the intron RNA plays no part (Dujon 1989;BellPedersen et al 1990;Belfort and Roberts 1997).…”

Section: Introductionmentioning

confidence: 99%

Activating the branch-forming splicing pathway by reengineering the ribozyme component of a natural group II intron

Monachello

Michel

Costa

2016

RNA

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When assayed in vitro, group IIC self-splicing introns, which target bacterial Rho-independent transcription terminators, generally fail to yield branched products during splicing despite their possessing a seemingly normal branchpoint. Starting with intron O.i.I1 from Oceanobacillus iheyensis, whose crystallographically determined structure lacks branchpoint-containing domain VI, we attempted to determine what makes this intron unfit for in vitro branch formation. A major factor was found to be the length of the helix at the base of domain VI: 4 base pairs (bp) are required for efficient branching, even though a majority of group IIC introns have a 3-bp helix. Equally important for lariat formation is the removal of interactions between ribozyme domains II and VI, which are specific to the second step of splicing. Conversely, mismatching of domain VI and its proposed first-step receptor in subdomain IC1 was found to be detrimental; these data suggest that the intron-encoded protein may promote branch formation partly by modulating the equilibrium between conformations specific to the first and second steps of splicing. As a practical application, we show that by making just two changes to the O.i.I1 ribozyme, it is possible to generate sufficient amounts of lariat intron for the latter to be purified and used in kinetic assays in which folding and reaction are uncoupled.

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“…A subset of filamentous fungal mt group IIB introns and a recently identified giant sulfur bacterial group IIC intron encode a LAGLIDADG DNA homing endonuclease instead of an RT (81,82,83,84). The LAGLIDADG ORF in the bacterial intron is located in DIV, whereas those in the fungal introns are located in DIII, indicating two separate insertions.…”

Section: Rt-independent Homingmentioning

confidence: 99%

Mobile Bacterial Group II Introns at the Crux of Eukaryotic Evolution

2015

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This review focuses on recent developments in our understanding of group II intron function, the relationships of these introns to retrotransposons and spliceosomes, and how their common features have informed thinking about bacterial group II introns as key elements in eukaryotic evolution. Reverse transcriptase-mediated and host factor-aided intron retrohoming pathways are considered along with retrotransposition mechanisms to novel sites in bacteria, where group II introns are thought to have originated. DNA target recognition and movement by target-primed reverse transcription infer an evolutionary relationship among group II introns, non-LTR retrotransposons, such as LINE elements, and telomerase. Additionally, group II introns are almost certainly the progenitors of spliceosomal introns. Their profound similarities include splicing chemistry extending to RNA catalysis, reaction stereochemistry, and the position of two divalent metals that perform catalysis at the RNA active site. There are also sequence and structural similarities between group II introns and the spliceosome's small nuclear RNAs (snRNAs) and between a highly conserved core spliceosomal protein Prp8 and a group II intron-like reverse transcriptase. It has been proposed that group II introns entered eukaryotes during bacterial endosymbiosis or bacterial-archaeal fusion, proliferated within the nuclear genome, necessitating evolution of the nuclear envelope, and fragmented giving rise to spliceosomal introns. Thus, these bacterial self-splicing mobile elements have fundamentally impacted the composition of extant eukaryotic genomes, including the human genome, most of which is derived from close relatives of mobile group II introns.

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

Cited by 67 publications

References 78 publications

Mobile Elements in a Single-Filament Orange Guaymas Basin Beggiatoa (“Candidatus Maribeggiatoa”) sp. Draft Genome: Evidence for Genetic Exchange with Cyanobacteria

Mobile Elements in a Single-Filament Orange Guaymas Basin Beggiatoa (“Candidatus Maribeggiatoa”) sp. Draft Genome: Evidence for Genetic Exchange with Cyanobacteria

Activating the branch-forming splicing pathway by reengineering the ribozyme component of a natural group II intron

Mobile Bacterial Group II Introns at the Crux of Eukaryotic Evolution

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