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The Ancient Evolutionary History of Polyomaviruses.

Buck CB, Van Doorslaer K, Peretti A, Geoghegan EM, Tisza MJ, An P, Katz JP, Pipas JM, McBride AA, Camus AC, McDermott AJ, Dill JA, Delwart E, Ng TF, Farkas K, Austin C, Kraberger S, Davison W, Pastrana DV, Varsani A - PLoS Pathog. (2016)

Bottom Line: To investigate the deeper evolutionary history of the family, we used a combination of viral metagenomics, bioinformatics, and structural modeling approaches to identify and characterize polyomavirus sequences associated with fish and arthropods.Phylogenetic analyses of individual polyomavirus genes suggest that some modern polyomavirus species arose after ancient recombination events involving distantly related polyomavirus lineages.The improved evolutionary model provides a useful platform for developing a more accurate taxonomic classification system for the viral family Polyomaviridae.

View Article: PubMed Central - PubMed

Affiliation: Lab of Cellular Oncology, NCI, NIH, Bethesda, Maryland, United States of America.

ABSTRACT
Polyomaviruses are a family of DNA tumor viruses that are known to infect mammals and birds. To investigate the deeper evolutionary history of the family, we used a combination of viral metagenomics, bioinformatics, and structural modeling approaches to identify and characterize polyomavirus sequences associated with fish and arthropods. Analyses drawing upon the divergent new sequences indicate that polyomaviruses have been gradually co-evolving with their animal hosts for at least half a billion years. Phylogenetic analyses of individual polyomavirus genes suggest that some modern polyomavirus species arose after ancient recombination events involving distantly related polyomavirus lineages. The improved evolutionary model provides a useful platform for developing a more accurate taxonomic classification system for the viral family Polyomaviridae.

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A hypothetical framework for ancient recombination events among major polyomavirus clades.The model attempts to reconcile observed incongruities between LT and VP1 phylogenetic trees shown in Figs 3 and 4. In the model, a hypothetical ancient polyomavirus, designated Arche, is inferred to have infected the last common ancestor of bilaterian animals. The ancient Arche lineage then gave rise to separate polyomavirus lineages found in arthropods and fish, as well as the mammalian Ortho/Almi lineages. The figure depicts Avi and Wuki clades arising after recombination events involving an unknown vertebrate-Arche lineage and Ortho-like species. The figure does not depict the inferred evolution of the HPyV6/7 clade, which appears to have arisen after a separate recombination event involving the late region of a hypothetical vertebrate-Arche lineage and the early region of a basal Almi-like species. The TSV lineage, which shows evidence of recombination between the Ortho and Almi lineages, is also omitted. White lollipops represent predicted pRb-binding motifs (LXCXE or related sequences). Yellow bars represent hypothetical metal-binding motifs (CXCXXC or related sequences). The absence of metal-binding motifs in Avi small T antigen (sT) proteins suggests a different evolutionary origin than the classic metal-binding Ortho/Almi sT. Possible ALTO-like ORFs predicted for some Ortho species are shaded gray.
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ppat.1005574.g005: A hypothetical framework for ancient recombination events among major polyomavirus clades.The model attempts to reconcile observed incongruities between LT and VP1 phylogenetic trees shown in Figs 3 and 4. In the model, a hypothetical ancient polyomavirus, designated Arche, is inferred to have infected the last common ancestor of bilaterian animals. The ancient Arche lineage then gave rise to separate polyomavirus lineages found in arthropods and fish, as well as the mammalian Ortho/Almi lineages. The figure depicts Avi and Wuki clades arising after recombination events involving an unknown vertebrate-Arche lineage and Ortho-like species. The figure does not depict the inferred evolution of the HPyV6/7 clade, which appears to have arisen after a separate recombination event involving the late region of a hypothetical vertebrate-Arche lineage and the early region of a basal Almi-like species. The TSV lineage, which shows evidence of recombination between the Ortho and Almi lineages, is also omitted. White lollipops represent predicted pRb-binding motifs (LXCXE or related sequences). Yellow bars represent hypothetical metal-binding motifs (CXCXXC or related sequences). The absence of metal-binding motifs in Avi small T antigen (sT) proteins suggests a different evolutionary origin than the classic metal-binding Ortho/Almi sT. Possible ALTO-like ORFs predicted for some Ortho species are shaded gray.

Mentions: Members of the previously recognized Wuki clade [29] encode VP1 protein sequences that occupy a highly divergent clade that distantly encompasses fish-associated VP1 sequences, while the early regions of Wuki species encode Ortho- or Almi-LT-like genes. Thus, relative to “classic” Ortho polyomaviruses the Avi clade shows a highly divergent early region while the Wuki clade shows a highly divergent late region. In Fig 5 we illustrate a recombination scheme that could account for this strangely mixed phylogeny.


The Ancient Evolutionary History of Polyomaviruses.

Buck CB, Van Doorslaer K, Peretti A, Geoghegan EM, Tisza MJ, An P, Katz JP, Pipas JM, McBride AA, Camus AC, McDermott AJ, Dill JA, Delwart E, Ng TF, Farkas K, Austin C, Kraberger S, Davison W, Pastrana DV, Varsani A - PLoS Pathog. (2016)

A hypothetical framework for ancient recombination events among major polyomavirus clades.The model attempts to reconcile observed incongruities between LT and VP1 phylogenetic trees shown in Figs 3 and 4. In the model, a hypothetical ancient polyomavirus, designated Arche, is inferred to have infected the last common ancestor of bilaterian animals. The ancient Arche lineage then gave rise to separate polyomavirus lineages found in arthropods and fish, as well as the mammalian Ortho/Almi lineages. The figure depicts Avi and Wuki clades arising after recombination events involving an unknown vertebrate-Arche lineage and Ortho-like species. The figure does not depict the inferred evolution of the HPyV6/7 clade, which appears to have arisen after a separate recombination event involving the late region of a hypothetical vertebrate-Arche lineage and the early region of a basal Almi-like species. The TSV lineage, which shows evidence of recombination between the Ortho and Almi lineages, is also omitted. White lollipops represent predicted pRb-binding motifs (LXCXE or related sequences). Yellow bars represent hypothetical metal-binding motifs (CXCXXC or related sequences). The absence of metal-binding motifs in Avi small T antigen (sT) proteins suggests a different evolutionary origin than the classic metal-binding Ortho/Almi sT. Possible ALTO-like ORFs predicted for some Ortho species are shaded gray.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4836724&req=5

ppat.1005574.g005: A hypothetical framework for ancient recombination events among major polyomavirus clades.The model attempts to reconcile observed incongruities between LT and VP1 phylogenetic trees shown in Figs 3 and 4. In the model, a hypothetical ancient polyomavirus, designated Arche, is inferred to have infected the last common ancestor of bilaterian animals. The ancient Arche lineage then gave rise to separate polyomavirus lineages found in arthropods and fish, as well as the mammalian Ortho/Almi lineages. The figure depicts Avi and Wuki clades arising after recombination events involving an unknown vertebrate-Arche lineage and Ortho-like species. The figure does not depict the inferred evolution of the HPyV6/7 clade, which appears to have arisen after a separate recombination event involving the late region of a hypothetical vertebrate-Arche lineage and the early region of a basal Almi-like species. The TSV lineage, which shows evidence of recombination between the Ortho and Almi lineages, is also omitted. White lollipops represent predicted pRb-binding motifs (LXCXE or related sequences). Yellow bars represent hypothetical metal-binding motifs (CXCXXC or related sequences). The absence of metal-binding motifs in Avi small T antigen (sT) proteins suggests a different evolutionary origin than the classic metal-binding Ortho/Almi sT. Possible ALTO-like ORFs predicted for some Ortho species are shaded gray.
Mentions: Members of the previously recognized Wuki clade [29] encode VP1 protein sequences that occupy a highly divergent clade that distantly encompasses fish-associated VP1 sequences, while the early regions of Wuki species encode Ortho- or Almi-LT-like genes. Thus, relative to “classic” Ortho polyomaviruses the Avi clade shows a highly divergent early region while the Wuki clade shows a highly divergent late region. In Fig 5 we illustrate a recombination scheme that could account for this strangely mixed phylogeny.

Bottom Line: To investigate the deeper evolutionary history of the family, we used a combination of viral metagenomics, bioinformatics, and structural modeling approaches to identify and characterize polyomavirus sequences associated with fish and arthropods.Phylogenetic analyses of individual polyomavirus genes suggest that some modern polyomavirus species arose after ancient recombination events involving distantly related polyomavirus lineages.The improved evolutionary model provides a useful platform for developing a more accurate taxonomic classification system for the viral family Polyomaviridae.

View Article: PubMed Central - PubMed

Affiliation: Lab of Cellular Oncology, NCI, NIH, Bethesda, Maryland, United States of America.

ABSTRACT
Polyomaviruses are a family of DNA tumor viruses that are known to infect mammals and birds. To investigate the deeper evolutionary history of the family, we used a combination of viral metagenomics, bioinformatics, and structural modeling approaches to identify and characterize polyomavirus sequences associated with fish and arthropods. Analyses drawing upon the divergent new sequences indicate that polyomaviruses have been gradually co-evolving with their animal hosts for at least half a billion years. Phylogenetic analyses of individual polyomavirus genes suggest that some modern polyomavirus species arose after ancient recombination events involving distantly related polyomavirus lineages. The improved evolutionary model provides a useful platform for developing a more accurate taxonomic classification system for the viral family Polyomaviridae.

Show MeSH
Related in: MedlinePlus