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Citation for Study 27000

Citation title: "Group II introns generate functional chimeric relaxase enzymes with modified specificities through exon shuffling at both the RNA and DNA level".

Study name: "Group II introns generate functional chimeric relaxase enzymes with modified specificities through exon shuffling at both the RNA and DNA level".

This study is part of submission 27000 (Status: Published).

Citation

Laroche-johnston F., Bosan R., & Cousineau B. 2020. Group II introns generate functional chimeric relaxase enzymes with modified specificities through exon shuffling at both the RNA and DNA level. Molecular Biology and Evolution, 38(3): 1075-1089.

Authors

• Laroche-johnston F. (submitter)
• Bosan R.
• Cousineau B.

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-LTR 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 most likely by recombination, can yield new functional enzymes with shuffled exons, which can lead to gain-of-function phenotypes.

Keywords

Group II introns, Lactococcus lactis, Enterococcus faecalis, Ll.LtrB, Ef.PcfG, conjugation, trans-splicing, bacterial genetics, genetic diversity, molecular evolution.

External links

• DOI: 10.1093/molbev/msaa275
• PMID: 33118013
• Other URL: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7947834/pdf/msaa275.pdf

About this resource

• Canonical resource URI: http://purl.org/phylo/treebase/phylows/study/TB2:S27000
• Other versions: Nexus NeXML
• Show BibTeX reference

  		@ARTICLE{TreeBASE2Ref31270,
  	 author = {Felix  LaRoche-Johnston and Rafia  Bosan and Benoit  Cousineau},
  	 title = {Group II introns generate functional chimeric relaxase enzymes with modified specificities through exon shuffling at both the RNA and DNA level},
  	 year = {2020},
  	 keywords = {Group II introns, Lactococcus lactis, Enterococcus faecalis, Ll.LtrB, Ef.PcfG, conjugation, trans-splicing, bacterial genetics, genetic diversity, molecular evolution.},
  	 doi = {10.1093/molbev/msaa275},
  	 url = {http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7947834/pdf/msaa275.pdf},
  	 pmid = {33118013},
  	 journal = {Molecular Biology and Evolution},
  	 volume = {38},
  	 number = {3},
  	 pages = {1075--1089},
  	 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-LTR 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 most likely by recombination, can yield new functional enzymes with shuffled exons, which can lead to gain-of-function phenotypes. }
  }
  		

• Show RIS reference

  		TY  - JOUR
  ID  - 31270
  AU  - LaRoche-Johnston,Felix 
  AU  - Bosan,Rafia 
  AU  - Cousineau,Benoit 
  T1  - Group II introns generate functional chimeric relaxase enzymes with modified specificities through exon shuffling at both the RNA and DNA level
  PY  - 2020
  KW  - Group II introns
  KW  - Lactococcus lactis
  KW  - Enterococcus faecalis
  KW  - Ll.LtrB
  KW  - Ef.PcfG
  KW  - conjugation
  KW  - trans-splicing
  KW  - bacterial genetics
  KW  - genetic diversity
  KW  - molecular evolution.
  UR  - http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7947834/pdf/msaa275.pdf
  N2  - 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-LTR 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 most likely by recombination, can yield new functional enzymes with shuffled exons, which can lead to gain-of-function phenotypes. 
  L3  - 10.1093/molbev/msaa275
  JF  - Molecular Biology and Evolution
  VL  - 38
  IS  - 3
  SP  - 1075
  EP  - 1089
  ER  -