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Evolution of eukaryotic single-stranded DNA viruses of the Bidnaviridae family from genes of four other groups of widely different viruses.

Krupovic M, Koonin EV - Sci Rep (2014)

Bottom Line: Our analysis strongly suggests that bidnaviruses evolved from a parvovirus ancestor from which they inherit a jelly-roll capsid protein and a superfamily 3 helicase.The radiation of bidnaviruses from parvoviruses was probably triggered by integration of the ancestral parvovirus genome into a large virus-derived DNA transposon of the Polinton (polintovirus) family resulting in the acquisition of the polintovirus PolB gene along with terminal inverted repeats.The unusual evolutionary history of bidnaviruses emphasizes the key role of horizontal gene transfer, sometimes between viruses with completely different genomes but occupying the same niche, in the emergence of new viral types.

View Article: PubMed Central - PubMed

Affiliation: Institut Pasteur, Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Department of Microbiology, Paris 75015, France.

ABSTRACT
Single-stranded (ss)DNA viruses are extremely widespread, infect diverse hosts from all three domains of life and include important pathogens. Most ssDNA viruses possess small genomes that replicate by the rolling-circle-like mechanism initiated by a distinct virus-encoded endonuclease. However, viruses of the family Bidnaviridae, instead of the endonuclease, encode a protein-primed type B DNA polymerase (PolB) and hence break this pattern. We investigated the provenance of all bidnavirus genes and uncover an unexpected turbulent evolutionary history of these unique viruses. Our analysis strongly suggests that bidnaviruses evolved from a parvovirus ancestor from which they inherit a jelly-roll capsid protein and a superfamily 3 helicase. The radiation of bidnaviruses from parvoviruses was probably triggered by integration of the ancestral parvovirus genome into a large virus-derived DNA transposon of the Polinton (polintovirus) family resulting in the acquisition of the polintovirus PolB gene along with terminal inverted repeats. Bidnavirus genes for a receptor-binding protein and a potential novel antiviral defense modulator are derived from dsRNA viruses (Reoviridae) and dsDNA viruses (Baculoviridae), respectively. The unusual evolutionary history of bidnaviruses emphasizes the key role of horizontal gene transfer, sometimes between viruses with completely different genomes but occupying the same niche, in the emergence of new viral types.

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Related in: MedlinePlus

Analysis of the major capsid protein of BmBDV.(a). Ribbon diagram of the X-ray structure of the capsid protein of Bombyx mori densovirus 1 (PDB ID: 3P0S)27. The core jelly-roll domain is highlighted in blue with the β-strands constituting the two β-sheets, BIDG and CHEF, indicated with corresponding letters. (b). Sequence alignment of the glycine-rich regions found in the N-termini of the parvoviral and bidnaviral capsid proteins. (c). Pairwise identity values between the sequences of capsid proteins of BmBDV and parvoviruses for which high-resolution structures are available. The accession numbers for the compared proteins are the same as in panel (d). (d). Multiple sequence alignment of the BmBDV and parvoviral capsid protein regions corresponding to the 8 β-strands forming the jelly-roll fold. The secondary structure elements of the BmBDV capsid protein were predicted using PSI-Pred57, whereas those of the parvoviral proteins were determined experimentally. Parvoviral sequences are indicated with their PDB accession numbers. Abbreviations: BmBDV-2, Bombyx mori bidensovirus 2; GmDNV, Galleria mellonella densovirus; AdDNV, Acheta domestica densovirus; BmDNV-1, Bombyx mori densovirus 1; CPV, canine parvovirus; MEV, mink enteritis virus; FPV, feline panleukopenia virus; PPV, porcine parvovirus; MVM, minute virus of mice; AAV-2, adeno-associated virus 2; HPV-B19, human parvovirus B19.
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f2: Analysis of the major capsid protein of BmBDV.(a). Ribbon diagram of the X-ray structure of the capsid protein of Bombyx mori densovirus 1 (PDB ID: 3P0S)27. The core jelly-roll domain is highlighted in blue with the β-strands constituting the two β-sheets, BIDG and CHEF, indicated with corresponding letters. (b). Sequence alignment of the glycine-rich regions found in the N-termini of the parvoviral and bidnaviral capsid proteins. (c). Pairwise identity values between the sequences of capsid proteins of BmBDV and parvoviruses for which high-resolution structures are available. The accession numbers for the compared proteins are the same as in panel (d). (d). Multiple sequence alignment of the BmBDV and parvoviral capsid protein regions corresponding to the 8 β-strands forming the jelly-roll fold. The secondary structure elements of the BmBDV capsid protein were predicted using PSI-Pred57, whereas those of the parvoviral proteins were determined experimentally. Parvoviral sequences are indicated with their PDB accession numbers. Abbreviations: BmBDV-2, Bombyx mori bidensovirus 2; GmDNV, Galleria mellonella densovirus; AdDNV, Acheta domestica densovirus; BmDNV-1, Bombyx mori densovirus 1; CPV, canine parvovirus; MEV, mink enteritis virus; FPV, feline panleukopenia virus; PPV, porcine parvovirus; MVM, minute virus of mice; AAV-2, adeno-associated virus 2; HPV-B19, human parvovirus B19.

Mentions: The virions of parvoviruses for which high resolution structural information is available, consist of homologous CPs that adopt the jelly-roll fold26272829. This fold is formed by two antiparallel β-sheets each consisting of four β-strands, BIDG and CHEF, respectively (Fig. 2a30). No homolog of the parvovirus CP has been thus far identified in BmBDV. However, given that the pairwise sequence identity between homologous parvoviral CPs is often about 5%28, the failure to establish the relationship between the CPs of BmBDV and other parvoviruses using standard BLAST search is not surprising.


Evolution of eukaryotic single-stranded DNA viruses of the Bidnaviridae family from genes of four other groups of widely different viruses.

Krupovic M, Koonin EV - Sci Rep (2014)

Analysis of the major capsid protein of BmBDV.(a). Ribbon diagram of the X-ray structure of the capsid protein of Bombyx mori densovirus 1 (PDB ID: 3P0S)27. The core jelly-roll domain is highlighted in blue with the β-strands constituting the two β-sheets, BIDG and CHEF, indicated with corresponding letters. (b). Sequence alignment of the glycine-rich regions found in the N-termini of the parvoviral and bidnaviral capsid proteins. (c). Pairwise identity values between the sequences of capsid proteins of BmBDV and parvoviruses for which high-resolution structures are available. The accession numbers for the compared proteins are the same as in panel (d). (d). Multiple sequence alignment of the BmBDV and parvoviral capsid protein regions corresponding to the 8 β-strands forming the jelly-roll fold. The secondary structure elements of the BmBDV capsid protein were predicted using PSI-Pred57, whereas those of the parvoviral proteins were determined experimentally. Parvoviral sequences are indicated with their PDB accession numbers. Abbreviations: BmBDV-2, Bombyx mori bidensovirus 2; GmDNV, Galleria mellonella densovirus; AdDNV, Acheta domestica densovirus; BmDNV-1, Bombyx mori densovirus 1; CPV, canine parvovirus; MEV, mink enteritis virus; FPV, feline panleukopenia virus; PPV, porcine parvovirus; MVM, minute virus of mice; AAV-2, adeno-associated virus 2; HPV-B19, human parvovirus B19.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4061559&req=5

f2: Analysis of the major capsid protein of BmBDV.(a). Ribbon diagram of the X-ray structure of the capsid protein of Bombyx mori densovirus 1 (PDB ID: 3P0S)27. The core jelly-roll domain is highlighted in blue with the β-strands constituting the two β-sheets, BIDG and CHEF, indicated with corresponding letters. (b). Sequence alignment of the glycine-rich regions found in the N-termini of the parvoviral and bidnaviral capsid proteins. (c). Pairwise identity values between the sequences of capsid proteins of BmBDV and parvoviruses for which high-resolution structures are available. The accession numbers for the compared proteins are the same as in panel (d). (d). Multiple sequence alignment of the BmBDV and parvoviral capsid protein regions corresponding to the 8 β-strands forming the jelly-roll fold. The secondary structure elements of the BmBDV capsid protein were predicted using PSI-Pred57, whereas those of the parvoviral proteins were determined experimentally. Parvoviral sequences are indicated with their PDB accession numbers. Abbreviations: BmBDV-2, Bombyx mori bidensovirus 2; GmDNV, Galleria mellonella densovirus; AdDNV, Acheta domestica densovirus; BmDNV-1, Bombyx mori densovirus 1; CPV, canine parvovirus; MEV, mink enteritis virus; FPV, feline panleukopenia virus; PPV, porcine parvovirus; MVM, minute virus of mice; AAV-2, adeno-associated virus 2; HPV-B19, human parvovirus B19.
Mentions: The virions of parvoviruses for which high resolution structural information is available, consist of homologous CPs that adopt the jelly-roll fold26272829. This fold is formed by two antiparallel β-sheets each consisting of four β-strands, BIDG and CHEF, respectively (Fig. 2a30). No homolog of the parvovirus CP has been thus far identified in BmBDV. However, given that the pairwise sequence identity between homologous parvoviral CPs is often about 5%28, the failure to establish the relationship between the CPs of BmBDV and other parvoviruses using standard BLAST search is not surprising.

Bottom Line: Our analysis strongly suggests that bidnaviruses evolved from a parvovirus ancestor from which they inherit a jelly-roll capsid protein and a superfamily 3 helicase.The radiation of bidnaviruses from parvoviruses was probably triggered by integration of the ancestral parvovirus genome into a large virus-derived DNA transposon of the Polinton (polintovirus) family resulting in the acquisition of the polintovirus PolB gene along with terminal inverted repeats.The unusual evolutionary history of bidnaviruses emphasizes the key role of horizontal gene transfer, sometimes between viruses with completely different genomes but occupying the same niche, in the emergence of new viral types.

View Article: PubMed Central - PubMed

Affiliation: Institut Pasteur, Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Department of Microbiology, Paris 75015, France.

ABSTRACT
Single-stranded (ss)DNA viruses are extremely widespread, infect diverse hosts from all three domains of life and include important pathogens. Most ssDNA viruses possess small genomes that replicate by the rolling-circle-like mechanism initiated by a distinct virus-encoded endonuclease. However, viruses of the family Bidnaviridae, instead of the endonuclease, encode a protein-primed type B DNA polymerase (PolB) and hence break this pattern. We investigated the provenance of all bidnavirus genes and uncover an unexpected turbulent evolutionary history of these unique viruses. Our analysis strongly suggests that bidnaviruses evolved from a parvovirus ancestor from which they inherit a jelly-roll capsid protein and a superfamily 3 helicase. The radiation of bidnaviruses from parvoviruses was probably triggered by integration of the ancestral parvovirus genome into a large virus-derived DNA transposon of the Polinton (polintovirus) family resulting in the acquisition of the polintovirus PolB gene along with terminal inverted repeats. Bidnavirus genes for a receptor-binding protein and a potential novel antiviral defense modulator are derived from dsRNA viruses (Reoviridae) and dsDNA viruses (Baculoviridae), respectively. The unusual evolutionary history of bidnaviruses emphasizes the key role of horizontal gene transfer, sometimes between viruses with completely different genomes but occupying the same niche, in the emergence of new viral types.

Show MeSH
Related in: MedlinePlus