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Evolution of DNA ligases of nucleo-cytoplasmic large DNA viruses of eukaryotes: a case of hidden complexity.
Biol Direct. 2009 Dec 18; 4:51.BD

Abstract

BACKGROUND

Eukaryotic Nucleo-Cytoplasmic Large DNA Viruses (NCLDV) encode most if not all of the enzymes involved in their DNA replication. It has been inferred that genes for these enzymes were already present in the last common ancestor of the NCLDV. However, the details of the evolution of these genes that bear on the complexity of the putative ancestral NCLDV and on the evolutionary relationships between viruses and their hosts are not well understood.

RESULTS

Phylogenetic analysis of the ATP-dependent and NAD-dependent DNA ligases encoded by the NCLDV reveals an unexpectedly complex evolutionary history. The NAD-dependent ligases are encoded only by a minority of NCLDV (including mimiviruses, some iridoviruses and entomopoxviruses) but phylogenetic analysis clearly indicated that all viral NAD-dependent ligases are monophyletic. Combined with the topology of the NCLDV tree derived by consensus of trees for universally conserved genes suggests that this enzyme was represented in the ancestral NCLDV. Phylogenetic analysis of ATP-dependent ligases that are encoded by chordopoxviruses, most of the phycodnaviruses and Marseillevirus failed to demonstrate monophyly and instead revealed an unexpectedly complex evolutionary trajectory. The ligases of the majority of phycodnaviruses and Marseillevirus seem to have evolved from bacteriophage or bacterial homologs; the ligase of one phycodnavirus, Emiliana huxlei virus, belongs to the eukaryotic DNA ligase I branch; and ligases of chordopoxviruses unequivocally cluster with eukaryotic DNA ligase III.

CONCLUSIONS

Examination of phyletic patterns and phylogenetic analysis of DNA ligases of the NCLDV suggest that the common ancestor of the extant NCLDV encoded an NAD-dependent ligase that most likely was acquired from a bacteriophage at the early stages of evolution of eukaryotes. By contrast, ATP-dependent ligases from different prokaryotic and eukaryotic sources displaced the ancestral NAD-dependent ligase at different stages of subsequent evolution. These findings emphasize complex routes of viral evolution that become apparent through detailed phylogenomic analysis but not necessarily in reconstructions based on phyletic patterns of genes.

REVIEWERS

This article was reviewed by: Patrick Forterre, George V. Shpakovski, and Igor B. Zhulin.

Authors+Show Affiliations

National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA. yutin@ncbi.nlm.nih.govNo affiliation info available

Pub Type(s)

Journal Article
Research Support, N.I.H., Intramural

Language

eng

PubMed ID

20021668

Citation

Yutin, Natalya, and Eugene V. Koonin. "Evolution of DNA Ligases of Nucleo-cytoplasmic Large DNA Viruses of Eukaryotes: a Case of Hidden Complexity." Biology Direct, vol. 4, 2009, p. 51.
Yutin N, Koonin EV. Evolution of DNA ligases of nucleo-cytoplasmic large DNA viruses of eukaryotes: a case of hidden complexity. Biol Direct. 2009;4:51.
Yutin, N., & Koonin, E. V. (2009). Evolution of DNA ligases of nucleo-cytoplasmic large DNA viruses of eukaryotes: a case of hidden complexity. Biology Direct, 4, 51. https://doi.org/10.1186/1745-6150-4-51
Yutin N, Koonin EV. Evolution of DNA Ligases of Nucleo-cytoplasmic Large DNA Viruses of Eukaryotes: a Case of Hidden Complexity. Biol Direct. 2009 Dec 18;4:51. PubMed PMID: 20021668.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Evolution of DNA ligases of nucleo-cytoplasmic large DNA viruses of eukaryotes: a case of hidden complexity. AU - Yutin,Natalya, AU - Koonin,Eugene V, Y1 - 2009/12/18/ PY - 2009/12/17/received PY - 2009/12/18/accepted PY - 2009/12/22/entrez PY - 2009/12/22/pubmed PY - 2010/3/5/medline SP - 51 EP - 51 JF - Biology direct JO - Biol Direct VL - 4 N2 - BACKGROUND: Eukaryotic Nucleo-Cytoplasmic Large DNA Viruses (NCLDV) encode most if not all of the enzymes involved in their DNA replication. It has been inferred that genes for these enzymes were already present in the last common ancestor of the NCLDV. However, the details of the evolution of these genes that bear on the complexity of the putative ancestral NCLDV and on the evolutionary relationships between viruses and their hosts are not well understood. RESULTS: Phylogenetic analysis of the ATP-dependent and NAD-dependent DNA ligases encoded by the NCLDV reveals an unexpectedly complex evolutionary history. The NAD-dependent ligases are encoded only by a minority of NCLDV (including mimiviruses, some iridoviruses and entomopoxviruses) but phylogenetic analysis clearly indicated that all viral NAD-dependent ligases are monophyletic. Combined with the topology of the NCLDV tree derived by consensus of trees for universally conserved genes suggests that this enzyme was represented in the ancestral NCLDV. Phylogenetic analysis of ATP-dependent ligases that are encoded by chordopoxviruses, most of the phycodnaviruses and Marseillevirus failed to demonstrate monophyly and instead revealed an unexpectedly complex evolutionary trajectory. The ligases of the majority of phycodnaviruses and Marseillevirus seem to have evolved from bacteriophage or bacterial homologs; the ligase of one phycodnavirus, Emiliana huxlei virus, belongs to the eukaryotic DNA ligase I branch; and ligases of chordopoxviruses unequivocally cluster with eukaryotic DNA ligase III. CONCLUSIONS: Examination of phyletic patterns and phylogenetic analysis of DNA ligases of the NCLDV suggest that the common ancestor of the extant NCLDV encoded an NAD-dependent ligase that most likely was acquired from a bacteriophage at the early stages of evolution of eukaryotes. By contrast, ATP-dependent ligases from different prokaryotic and eukaryotic sources displaced the ancestral NAD-dependent ligase at different stages of subsequent evolution. These findings emphasize complex routes of viral evolution that become apparent through detailed phylogenomic analysis but not necessarily in reconstructions based on phyletic patterns of genes. REVIEWERS: This article was reviewed by: Patrick Forterre, George V. Shpakovski, and Igor B. Zhulin. SN - 1745-6150 UR - https://www.unboundmedicine.com/medline/citation/20021668/Evolution_of_DNA_ligases_of_nucleo_cytoplasmic_large_DNA_viruses_of_eukaryotes:_a_case_of_hidden_complexity_ L2 - https://biologydirect.biomedcentral.com/articles/10.1186/1745-6150-4-51 DB - PRIME DP - Unbound Medicine ER -