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DNA transposons have colonized the genome of the giant virus Pandoravirus salinus.

Sun C, Feschotte C, Wu Z, Mueller RL - BMC Biol. (2015)

Bottom Line: These observations suggest that the Submariner MITEs of P. salinus belong to the widespread Tc1/mariner superfamily and may have been mobilized by an amoebozoan host.Ten of the 30 MITEs in the P. salinus genome are located within coding regions of predicted genes, while others are close to genes, suggesting that these transposons may have contributed to viral genetic novelty.Our findings continue to blur the division between viral and cellular genomes, adhering to the emerging view that the content, dynamics, and evolution of the genomes of giant viruses do not substantially differ from those of cellular organisms.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Colorado State University, Campus Delivery 1878, Fort Collins, CO, 80523-1878, USA. transposable.element@gmail.com.

ABSTRACT

Background: Transposable elements are mobile DNA sequences that are widely distributed in prokaryotic and eukaryotic genomes, where they represent a major force in genome evolution. However, transposable elements have rarely been documented in viruses, and their contribution to viral genome evolution remains largely unexplored. Pandoraviruses are recently described DNA viruses with genome sizes that exceed those of some prokaryotes, rivaling parasitic eukaryotes. These large genomes appear to include substantial noncoding intergenic spaces, which provide potential locations for transposable element insertions. However, no mobile genetic elements have yet been reported in pandoravirus genomes.

Results: Here, we report a family of miniature inverted-repeat transposable elements (MITEs) in the Pandoravirus salinus genome, representing the first description of a virus populated with a canonical transposable element family that proliferated by transposition within the viral genome. The MITE family, which we name Submariner, includes 30 copies with all the hallmarks of MITEs: short length, terminal inverted repeats, TA target site duplication, and no coding capacity. Submariner elements show signs of transposition and are undetectable in the genome of Pandoravirus dulcis, the closest known relative Pandoravirus salinus. We identified a DNA transposon related to Submariner in the genome of Acanthamoeba castellanii, a species thought to host pandoraviruses, which contains remnants of coding sequence for a Tc1/mariner transposase. These observations suggest that the Submariner MITEs of P. salinus belong to the widespread Tc1/mariner superfamily and may have been mobilized by an amoebozoan host. Ten of the 30 MITEs in the P. salinus genome are located within coding regions of predicted genes, while others are close to genes, suggesting that these transposons may have contributed to viral genetic novelty.

Conclusions: Our discovery highlights the remarkable ability of DNA transposons to colonize and shape genomes from all domains of life, as well as giant viruses. Our findings continue to blur the division between viral and cellular genomes, adhering to the emerging view that the content, dynamics, and evolution of the genomes of giant viruses do not substantially differ from those of cellular organisms.

No MeSH data available.


Related in: MedlinePlus

Autonomous DNA transposon in the amoeba Acanthamoeba castellanii that is closely related to the MITEs in P. salinus.a Pairwise alignment of the flanking sequences of the DNA transposon insertion and a paralogous empty site elsewhere in the A. castellanii genome. Red bar indicates the transposon insertion site. Bold and underlined letters (TA) indicate TSD. The paralogous empty site is evidence of transposition. b The structure of the autonomous DNA transposon in A. castellanii. Triangles indicate TIRs. Stars indicate stop codons in the putative transposase sequence. c Alignment of the ends of the consensus sequence of the MITEs in P. salinus and the ends of the autonomous DNA transposon sequence in A. castellanii, referred to as Submariner_Ac1. TIRs for each element are boxed. Columns in the alignment are shaded when nucleotides are conserved in at least three sequences. RC stands for reverse-complement. The sequence similarity between the TIRs of the P. salinus MITE and the A. castellanii DNA transposon Submariner_Ac1 indicates that the P. salinus MITE could have been cross-mobilized in the viral genome by the A. castellanii DNA transposon
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Fig2: Autonomous DNA transposon in the amoeba Acanthamoeba castellanii that is closely related to the MITEs in P. salinus.a Pairwise alignment of the flanking sequences of the DNA transposon insertion and a paralogous empty site elsewhere in the A. castellanii genome. Red bar indicates the transposon insertion site. Bold and underlined letters (TA) indicate TSD. The paralogous empty site is evidence of transposition. b The structure of the autonomous DNA transposon in A. castellanii. Triangles indicate TIRs. Stars indicate stop codons in the putative transposase sequence. c Alignment of the ends of the consensus sequence of the MITEs in P. salinus and the ends of the autonomous DNA transposon sequence in A. castellanii, referred to as Submariner_Ac1. TIRs for each element are boxed. Columns in the alignment are shaded when nucleotides are conserved in at least three sequences. RC stands for reverse-complement. The sequence similarity between the TIRs of the P. salinus MITE and the A. castellanii DNA transposon Submariner_Ac1 indicates that the P. salinus MITE could have been cross-mobilized in the viral genome by the A. castellanii DNA transposon

Mentions: To investigate whether the 1604 bp sequence has been transpositionally active, we looked for paralogous empty sites within the A. castellanii genome. To this end, we used 100 bp of sequence flanking the 1604 bp sequence on either side as queries to BLASTn against the total genomic sequences of A. castellanii. We found one paralogous empty site (Fig. 2a and Additional file 5: Figure S5), confirming transposition activity of the 1604 bp sequence (sequence divergence between the empty site and its paralog containing the 1604 bp sequence is approximately 6 % over 121 bp; e-value = 1e-67). Integration of the new 1604 bp sequence generated a 5′-TA-3′ TSD (Fig. 2a), suggesting that the sequence has a typical TSD of a Tc1/mariner superfamily DNA transposon.Fig. 2


DNA transposons have colonized the genome of the giant virus Pandoravirus salinus.

Sun C, Feschotte C, Wu Z, Mueller RL - BMC Biol. (2015)

Autonomous DNA transposon in the amoeba Acanthamoeba castellanii that is closely related to the MITEs in P. salinus.a Pairwise alignment of the flanking sequences of the DNA transposon insertion and a paralogous empty site elsewhere in the A. castellanii genome. Red bar indicates the transposon insertion site. Bold and underlined letters (TA) indicate TSD. The paralogous empty site is evidence of transposition. b The structure of the autonomous DNA transposon in A. castellanii. Triangles indicate TIRs. Stars indicate stop codons in the putative transposase sequence. c Alignment of the ends of the consensus sequence of the MITEs in P. salinus and the ends of the autonomous DNA transposon sequence in A. castellanii, referred to as Submariner_Ac1. TIRs for each element are boxed. Columns in the alignment are shaded when nucleotides are conserved in at least three sequences. RC stands for reverse-complement. The sequence similarity between the TIRs of the P. salinus MITE and the A. castellanii DNA transposon Submariner_Ac1 indicates that the P. salinus MITE could have been cross-mobilized in the viral genome by the A. castellanii DNA transposon
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4495683&req=5

Fig2: Autonomous DNA transposon in the amoeba Acanthamoeba castellanii that is closely related to the MITEs in P. salinus.a Pairwise alignment of the flanking sequences of the DNA transposon insertion and a paralogous empty site elsewhere in the A. castellanii genome. Red bar indicates the transposon insertion site. Bold and underlined letters (TA) indicate TSD. The paralogous empty site is evidence of transposition. b The structure of the autonomous DNA transposon in A. castellanii. Triangles indicate TIRs. Stars indicate stop codons in the putative transposase sequence. c Alignment of the ends of the consensus sequence of the MITEs in P. salinus and the ends of the autonomous DNA transposon sequence in A. castellanii, referred to as Submariner_Ac1. TIRs for each element are boxed. Columns in the alignment are shaded when nucleotides are conserved in at least three sequences. RC stands for reverse-complement. The sequence similarity between the TIRs of the P. salinus MITE and the A. castellanii DNA transposon Submariner_Ac1 indicates that the P. salinus MITE could have been cross-mobilized in the viral genome by the A. castellanii DNA transposon
Mentions: To investigate whether the 1604 bp sequence has been transpositionally active, we looked for paralogous empty sites within the A. castellanii genome. To this end, we used 100 bp of sequence flanking the 1604 bp sequence on either side as queries to BLASTn against the total genomic sequences of A. castellanii. We found one paralogous empty site (Fig. 2a and Additional file 5: Figure S5), confirming transposition activity of the 1604 bp sequence (sequence divergence between the empty site and its paralog containing the 1604 bp sequence is approximately 6 % over 121 bp; e-value = 1e-67). Integration of the new 1604 bp sequence generated a 5′-TA-3′ TSD (Fig. 2a), suggesting that the sequence has a typical TSD of a Tc1/mariner superfamily DNA transposon.Fig. 2

Bottom Line: These observations suggest that the Submariner MITEs of P. salinus belong to the widespread Tc1/mariner superfamily and may have been mobilized by an amoebozoan host.Ten of the 30 MITEs in the P. salinus genome are located within coding regions of predicted genes, while others are close to genes, suggesting that these transposons may have contributed to viral genetic novelty.Our findings continue to blur the division between viral and cellular genomes, adhering to the emerging view that the content, dynamics, and evolution of the genomes of giant viruses do not substantially differ from those of cellular organisms.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Colorado State University, Campus Delivery 1878, Fort Collins, CO, 80523-1878, USA. transposable.element@gmail.com.

ABSTRACT

Background: Transposable elements are mobile DNA sequences that are widely distributed in prokaryotic and eukaryotic genomes, where they represent a major force in genome evolution. However, transposable elements have rarely been documented in viruses, and their contribution to viral genome evolution remains largely unexplored. Pandoraviruses are recently described DNA viruses with genome sizes that exceed those of some prokaryotes, rivaling parasitic eukaryotes. These large genomes appear to include substantial noncoding intergenic spaces, which provide potential locations for transposable element insertions. However, no mobile genetic elements have yet been reported in pandoravirus genomes.

Results: Here, we report a family of miniature inverted-repeat transposable elements (MITEs) in the Pandoravirus salinus genome, representing the first description of a virus populated with a canonical transposable element family that proliferated by transposition within the viral genome. The MITE family, which we name Submariner, includes 30 copies with all the hallmarks of MITEs: short length, terminal inverted repeats, TA target site duplication, and no coding capacity. Submariner elements show signs of transposition and are undetectable in the genome of Pandoravirus dulcis, the closest known relative Pandoravirus salinus. We identified a DNA transposon related to Submariner in the genome of Acanthamoeba castellanii, a species thought to host pandoraviruses, which contains remnants of coding sequence for a Tc1/mariner transposase. These observations suggest that the Submariner MITEs of P. salinus belong to the widespread Tc1/mariner superfamily and may have been mobilized by an amoebozoan host. Ten of the 30 MITEs in the P. salinus genome are located within coding regions of predicted genes, while others are close to genes, suggesting that these transposons may have contributed to viral genetic novelty.

Conclusions: Our discovery highlights the remarkable ability of DNA transposons to colonize and shape genomes from all domains of life, as well as giant viruses. Our findings continue to blur the division between viral and cellular genomes, adhering to the emerging view that the content, dynamics, and evolution of the genomes of giant viruses do not substantially differ from those of cellular organisms.

No MeSH data available.


Related in: MedlinePlus