Distinct Expansion of Group II Introns Depends on the Type of Intron-encoded Protein and Genomic Signatures in Prokaryotes

AbstractGroup II introns (G2Is) are self-splicing ribozymes that have retroelement characteristics in prokaryotes. Although G2Is are considered an important factor in the evolution of prokaryotes, comprehensive analyses of these introns among the tens of thousands of prokaryotic genomes currently available are still limited. Here, we developed a bioinformatic pipeline that systematically collects G2Is and applied it to prokaryotic genomes. We found that in bacteria, 25% (447 of 1,790) of the total representative species had an average of 5.3 G2Is, and in archaea, 9% (28 of 296) of the total representative species had an average of 3.0 G2Is. The greatest number of G2Is per species was 101 in Arthrospira platensis (phylum Cyanobacteriota). A comprehensive sequence analysis of the intron-encoded protein (IEP) in each G2I sequence was conducted and resulted in the addition of three new IEP classes (U1–U3) to the previous classification. This analysis suggested that about 30% of all IEPs are noncanonical IEPs. The number of G2Is per species was defined almost at the phylum level, and the type of IEP was associated as a factor in the G2I increase, i.e. there was an explosive increase in G2Is with bacterial C-type IEPs in the phylum Firmicutes and in G2Is with CL-type IEPs in the phylum Cyanobacteriota. We also systematically analyzed the relationship between genomic signatures and the mechanism of these increases in G2Is. This is the first study to systematically characterize G2Is in the prokaryotic phylogenies.

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Self‐Splicing Group II Introns

Ribozymes ◽

10.1002/9783527814527.ch6 ◽

2021 ◽

pp. 143-167

Author(s):

Isabel Chillón ◽

Marco Marcia

Keyword(s):

Group Ii Introns ◽

Group Ii ◽

Self Splicing

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Group II intron as cold sensor for self-preservation and bacterial conjugation

Nucleic Acids Research ◽

10.1093/nar/gkaa313 ◽

2020 ◽

Vol 48 (11) ◽

pp. 6198-6209 ◽

Cited By ~ 1

Author(s):

Xiaolong Dong ◽

Guosheng Qu ◽

Carol Lyn Piazza ◽

Marlene Belfort

Keyword(s):

Group Ii Intron ◽

Cold Sensitivity ◽

Group Ii Introns ◽

Intron Splicing ◽

Kinetic Trap ◽

Group Ii ◽

Self Splicing ◽

Mrna Targeting ◽

Cold Sensor

Abstract Group II introns are self-splicing ribozymes and mobile genetic elements. Splicing is required for both expression of the interrupted host gene and intron retromobility. For the pRS01 plasmid-encoded Lactococcus lactis group II intron, Ll.LtrB, splicing enables expression of the intron's host relaxase protein. Relaxase, in turn, initiates horizontal transfer of the conjugative pRS01 plasmid and stimulates retrotransposition of the intron. Little is known about how splicing of bacterial group II introns is influenced by environmental conditions. Here, we show that low temperatures can inhibit Ll.LtrB intron splicing. Whereas autocatalysis is abolished in the cold, splicing is partially restored by the intron-encoded protein (IEP). Structure profiling reveals cold-induced disruptions of key tertiary interactions, suggesting that a kinetic trap prevents the intron RNA from assuming its native state. Interestingly, while reduced levels of transcription and splicing lead to a paucity of excised intron in the cold, levels of relaxase mRNA are maintained, partially due to diminished intron-mediated mRNA targeting, allowing intron spread by conjugal transfer. Taken together, this study demonstrates not only the intrinsic cold sensitivity of group II intron splicing and the role of the IEP for cold-stress adaptation, but also maintenance of horizontal plasmid and intron transfer under cold-shock.

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Self-splicing of group II introns in vitro: Mapping of the branch point and mutational inhibition of lariat formation

Cell ◽

10.1016/0092-8674(86)90881-0 ◽

1986 ◽

Vol 46 (4) ◽

pp. 557-565 ◽

Cited By ~ 117

Author(s):

Carlo Schmelzer ◽

Rudolf J. Schweyen

Keyword(s):

Branch Point ◽

Group Ii Introns ◽

Group Ii ◽

Self Splicing

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Group II introns deleted for multiple substructures retain self-splicing activity

Molecular and Cellular Biology ◽

10.1128/mcb.12.5.1950-1958.1992 ◽

1992 ◽

Vol 12 (5) ◽

pp. 1950-1958

Author(s):

J L Koch ◽

S C Boulanger ◽

S D Dib-Hajj ◽

S K Hebbar ◽

P S Perlman

Keyword(s):

Binding Site ◽

Splice Junction ◽

Group Ii Introns ◽

Splice Site Selection ◽

Catalytic Core ◽

Single Deletion ◽

Group Ii ◽

Precursor Rna ◽

Self Splicing

Group II introns can be folded into highly conserved secondary structures with six major substructures or domains. Domains 1 and 5 are known to play key roles in self-splicing, while the roles of domains 2, 3, 4, and 6 are less clear. A trans assay for domain 5 function has been developed which indicates that domain 5 has a binding site on the precursor RNA that is not predicted from any secondary structure element. In this study, the self-splicing group II intron 5 gamma of the coxI gene of yeast mitochondrial DNA was deleted for various intron domains, singly and in combinations. Those mutant introns were characterized for self-splicing reactions in vitro as a means of locating the domain 5 binding site. A single deletion of domain 2, 3, 4, or 6 does not block in vitro reactions at either splice junction, though the deletion of domain 6 reduces the fidelity of 3' splice site selection somewhat. Even the triple deletion lacking domains 2, 4, and 6 retains some self-splicing activity. The deletion of domains 2, 3, 4, and 6 blocks the reaction at the 3' splice junction but not at the 5' junction. From these results, we conclude that the binding site for domain 5 is within domain 1 and that the complex of 5' exon, domain 1, and domain 5 (plus short connecting sequences) constitutes the essential catalytic core of this intron.

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