scholarly journals Recent mobility of plastid encoded group II introns and twintrons in five strains of the unicellular red alga Porphyridium

Author(s):  
Marie-Mathilde Perrineau ◽  
Dana C Price ◽  
Georg Mohr ◽  
Debashish Bhattacharya

Group II introns are closely linked to eukaryote evolution because nuclear spliceosomal introns and the small RNAs associated with the spliceosome are thought to trace their ancient origins to these mobile elements. Therefore, elucidating how group II introns move, and how they lose mobility can potentially shed light on fundamental aspects of eukaryote biology. To this end, we studied five strains of the unicellular red alga Porphyridium purpureum that surprisingly contain 42 group II introns in their plastid genomes. We focused on a subset of these introns that encode mobility-conferring intron-encoded proteins (IEPs) and found them to be distributed among the strains in a lineage-specific manner. The reverse transcriptase and maturase domains were present in all lineages but the DNA endonuclease domain was deleted in vertically inherited introns, demonstrating a key step in the loss of mobility. P. purpureum plastid intron RNAs had a classic group IIB secondary structure despite variability in the DIII and DVI domains. We report for the first time the presence of twintrons (introns-within-introns, derived from the same mobile element) in Rhodophyta. The P. purpureum IEPs and their mobile introns provide a valuable model for the study of mobile retroelements in eukaryotes and offer promise for biotechnological applications.

2014 ◽  
Author(s):  
Marie-Mathilde Perrineau ◽  
Dana C Price ◽  
Georg Mohr ◽  
Debashish Bhattacharya

Group II introns are closely linked to eukaryote evolution because nuclear spliceosomal introns and the small RNAs associated with the spliceosome are thought to trace their ancient origins to these mobile elements. Therefore, elucidating how group II introns move, and how they lose mobility can potentially shed light on fundamental aspects of eukaryote biology. To this end, we studied five strains of the unicellular red alga Porphyridium purpureum that surprisingly contain 42 group II introns in their plastid genomes. We focused on a subset of these introns that encode mobility-conferring intron-encoded proteins (IEPs) and found them to be distributed among the strains in a lineage-specific manner. The reverse transcriptase and maturase domains were present in all lineages but the DNA endonuclease domain was deleted in vertically inherited introns, demonstrating a key step in the loss of mobility. P. purpureum plastid intron RNAs had a classic group IIB secondary structure despite variability in the DIII and DVI domains. We report for the first time the presence of twintrons (introns-within-introns, derived from the same mobile element) in Rhodophyta. The P. purpureum IEPs and their mobile introns provide a valuable model for the study of mobile retroelements in eukaryotes and offer promise for biotechnological applications.


eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Guosheng Qu ◽  
Carol Lyn Piazza ◽  
Dorie Smith ◽  
Marlene Belfort

Group II introns are mobile ribozymes that are rare in bacterial genomes, often cohabiting with various mobile elements, and seldom interrupting housekeeping genes. What accounts for this distribution has not been well understood. Here, we demonstrate that Ll.LtrB, the group II intron residing in a relaxase gene on a conjugative plasmid from Lactococcus lactis, inhibits its host gene expression and restrains the naturally cohabiting mobile element from conjugative horizontal transfer. We show that reduction in gene expression is mainly at the mRNA level, and results from the interaction between exon-binding sequences (EBSs) in the intron and intron-binding sequences (IBSs) in the mRNA. The spliced intron targets the relaxase mRNA and reopens ligated exons, causing major mRNA loss. Taken together, this study provides an explanation for the distribution and paucity of group II introns in bacteria, and suggests a potential force for those introns to evolve into spliceosomal introns.


Author(s):  
María Dolores Molina-Sánchez ◽  
Rafael Nisa-Martínez ◽  
Fernando M. García-Rodríguez ◽  
Francisco Martínez-Abarca ◽  
Nicolás Toro

BMC Biology ◽  
2022 ◽  
Vol 20 (1) ◽  
Author(s):  
Dongseok Kim ◽  
JunMo Lee ◽  
Chung Hyun Cho ◽  
Eun Jeung Kim ◽  
Debashish Bhattacharya ◽  
...  

Abstract Background Group II introns are mobile genetic elements that can insert at specific target sequences, however, their origins are often challenging to reconstruct because of rapid sequence decay following invasion and spread into different sites. To advance understanding of group II intron spread, we studied the intron-rich mitochondrial genome (mitogenome) in the unicellular red alga, Porphyridium. Results Analysis of mitogenomes in three closely related species in this genus revealed they were 3–6-fold larger in size (56–132 kbp) than in other red algae, that have genomes of size 21–43 kbp. This discrepancy is explained by two factors, group II intron invasion and expansion of repeated sequences in large intergenic regions. Phylogenetic analysis demonstrates that many mitogenome group II intron families are specific to Porphyridium, whereas others are closely related to sequences in fungi and in the red alga-derived plastids of stramenopiles. Network analysis of intron-encoded proteins (IEPs) shows a clear link between plastid and mitochondrial IEPs in distantly related species, with both groups associated with prokaryotic sequences. Conclusion Our analysis of group II introns in Porphyridium mitogenomes demonstrates the dynamic nature of group II intron evolution, strongly supports the lateral movement of group II introns among diverse eukaryotes, and reveals their ability to proliferate, once integrated in mitochondrial DNA.


Author(s):  
Félix LaRoche-Johnston ◽  
Rafia Bosan ◽  
Benoit Cousineau

Abstract Group II introns are large self-splicing RNA enzymes with a broad but somewhat irregular phylogenetic distribution. These ancient retromobile elements are the proposed ancestors of approximately half the human genome, including the abundant spliceosomal introns and non-long terminal repeat retrotransposons. In contrast to their eukaryotic derivatives, bacterial group II introns have largely been considered as harmful selfish mobile retroelements that parasitize the genome of their host. As a challenge to this view, we recently uncovered a new intergenic trans-splicing pathway that generates an assortment of mRNA chimeras. The ability of group II introns to combine disparate mRNA fragments was proposed to increase the genetic diversity of the bacterial host by shuffling coding sequences. Here, we show that the Ll.LtrB and Ef.PcfG group II introns from Lactococcus lactis and Enterococcus faecalis respectively can both use the intergenic trans-splicing pathway to catalyze the formation of chimeric relaxase mRNAs and functional proteins. We demonstrated that some of these compound relaxase enzymes yield gain-of-function phenotypes, being significantly more efficient than their precursor wild-type enzymes at supporting bacterial conjugation. We also found that relaxase enzymes with shuffled functional domains are produced in biologically relevant settings under natural expression levels. Finally, we uncovered examples of lactococcal chimeric relaxase genes with junctions exactly at the intron insertion site. Overall, our work demonstrates that the genetic diversity generated by group II introns, at the RNA level by intergenic trans-splicing and at the DNA level by recombination, can yield new functional enzymes with shuffled exons, which can lead to gain-of-function phenotypes.


2018 ◽  
Vol 22 ◽  
pp. 345-351
Author(s):  
O. V. Pidpala ◽  
L. L. Lukash

Aim. The intron sequences of orthologous О6-methylguanin-DNA methyltransferase (MGMT) genes in Protists on the early stages of their formation in eukaryotic organisms have been analysed. Methods. Homologous regions have been defined by the program BLASTN 2.6.1. Nucleotide sequences of the bacterial and mitochondrial group II introns have been taken from Database for Bacterial Group II Introns. Searching and identifying the MGEs have been realized by using CENSOR. Results. It has been shown that the evolution of the gene does not always coincide with the evolution of the organism. This is shown on the example of intron loss and gain in social amoebae Dictyostelium. Also it has been found the fragmentary nature of homology between various introns and exons of the orthologous genes. Conclusions. The obtained results allow offer a suggestion about the endogenous mosaic character of the evolutional formation of the gene structural units. Keywords: О6-methylguanin-DNA methyltransferase (MGMT) gene orthologous, Protists, gene evolution, spliceosomal introns, intron loss and gain.


2021 ◽  
Vol 22 (20) ◽  
pp. 11139
Author(s):  
Ewa Górecka ◽  
Romain Gastineau ◽  
Nikolai A. Davidovich ◽  
Olga I. Davidovich ◽  
Matt P. Ashworth ◽  
...  

We provide for the first time the complete plastid and mitochondrial genomes of a monoraphid diatom: Schizostauron trachyderma. The mitogenome is 41,957 bp in size and displays two group II introns in the cox1 gene. The 187,029 bp plastid genome features the typical quadripartite architecture of diatom genomes. It contains a group II intron in the petB gene that overlaps the large single-copy and the inverted repeat region. There is also a group IB4 intron encoding a putative LAGLIDADG homing endonuclease in the rnl gene. The multigene phylogenies conducted provide more evidence of the proximity between S. trachyderma and fistula-bearing species of biraphid diatoms.


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