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Evolution of DNA ligases of nucleo-cytoplasmic large DNA viruses of eukaryotes: a case of hidden complexity.

Yutin N, Koonin EV - Biol. Direct (2009)

Bottom Line: 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.Shpakovski, and Igor B.Zhulin.

View Article: PubMed Central - HTML - PubMed

Affiliation: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA. yutin@ncbi.nlm.nih.gov

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.

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Related in: MedlinePlus

A maximum-likelihood phylogenetic tree of NAD-dependent DNA ligases. The numbers indicate the statistical support (Expected-Likelihood Weights) of internal nodes. The support values are given as percentages (n = 1,000). Archaeal sequences are color-coded red, bacterial sequences green, eukaryotic sequences brown, and viral sequences blue. The NCLDV are shown in bold type. All proteins are denoted by their Genbank identification numbers (GIs). The truncated sequence of the NAD-dependent ligase of Crocodilepox virus was not used for phylogenetic analysis. Abbreviations: MSV, Melanoplus sanguinipes entomopoxvirus; AMV, Amsacta moorei entomopoxvirus; Acapo, Acanthamoeba polyphaga mimivirus; CIV, Chilo iridescent virus (Invertebrate iridescent virus 6); Aedta, Aedes taeniorhynchus iridescent virus (Invertebrate iridescent virus 3); Ralph, Ralstonia solanacearum phage RSL1; Lenar, Lentisphaera araneosa HTCC2155; Acife, Acidithiobacillus ferrooxidans ATCC 23270; Marsp, Marinobacter sp. ELB17; Desal, Desulfatibacillum alkenivorans AK-01; Desac, Desulfuromonas acetoxidans DSM 684; Natph, Natronomonas pharaonis DSM 2160; Halwa, Haloquadratum walsbyi DSM 16790; Ostlu, Ostreococcus lucimarinus CCE9901; Ricfe, Rickettsia felis URRWXCal2; Metin, Methylacidiphilum infernorum V4; Nitsp, Nitratiruptor sp. SB155-2; Aquae, Aquifex aeolicus VF5; CanBl, Candidatus Blochmannia floridanus; Brahy, Brachyspira hyodysenteriae WA1; Lepbu, Leptotrichia buccalis DSM 1135; Dicdi, Dictyostelium discoideum AX4; Borhe, Borrelia hermsii DAH; Bacth, Bacillus thuringiensis Bt407; Cloca, Clostridium carboxidivorans P7; Plepa, Plesiocystis pacifica SIR-1; Sorce, Sorangium cellulosum.
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Figure 1: A maximum-likelihood phylogenetic tree of NAD-dependent DNA ligases. The numbers indicate the statistical support (Expected-Likelihood Weights) of internal nodes. The support values are given as percentages (n = 1,000). Archaeal sequences are color-coded red, bacterial sequences green, eukaryotic sequences brown, and viral sequences blue. The NCLDV are shown in bold type. All proteins are denoted by their Genbank identification numbers (GIs). The truncated sequence of the NAD-dependent ligase of Crocodilepox virus was not used for phylogenetic analysis. Abbreviations: MSV, Melanoplus sanguinipes entomopoxvirus; AMV, Amsacta moorei entomopoxvirus; Acapo, Acanthamoeba polyphaga mimivirus; CIV, Chilo iridescent virus (Invertebrate iridescent virus 6); Aedta, Aedes taeniorhynchus iridescent virus (Invertebrate iridescent virus 3); Ralph, Ralstonia solanacearum phage RSL1; Lenar, Lentisphaera araneosa HTCC2155; Acife, Acidithiobacillus ferrooxidans ATCC 23270; Marsp, Marinobacter sp. ELB17; Desal, Desulfatibacillum alkenivorans AK-01; Desac, Desulfuromonas acetoxidans DSM 684; Natph, Natronomonas pharaonis DSM 2160; Halwa, Haloquadratum walsbyi DSM 16790; Ostlu, Ostreococcus lucimarinus CCE9901; Ricfe, Rickettsia felis URRWXCal2; Metin, Methylacidiphilum infernorum V4; Nitsp, Nitratiruptor sp. SB155-2; Aquae, Aquifex aeolicus VF5; CanBl, Candidatus Blochmannia floridanus; Brahy, Brachyspira hyodysenteriae WA1; Lepbu, Leptotrichia buccalis DSM 1135; Dicdi, Dictyostelium discoideum AX4; Borhe, Borrelia hermsii DAH; Bacth, Bacillus thuringiensis Bt407; Cloca, Clostridium carboxidivorans P7; Plepa, Plesiocystis pacifica SIR-1; Sorce, Sorangium cellulosum.

Mentions: To reconstruct the evolutionary scenario for viral ligases, we used multiple alignments of the NAD-dependent and ATP-dependent ligases that included the respective protein sequences from the NCLDV, other viruses, and representative archaea, bacteria, and eukaryotes (see Additional File 1 and Additional File 2, respectively), to build maximum likelihood (ML) phylogenetic trees. The tree for the NAD-dependent ligases contains an unequivocally supported NCLDV clade (Figure 1). Statistical evaluation of alternative tree topologies using the Approximately Unbiased (AU) test [22] indicated that trees with polyphyletic NCLDV effectively could be ruled out (all these alternative topologies had zero AU values). The NCLDV clade belonged to a branch that included mostly NAD-dependent ligases from gamma-proteobacteria along with some bacteriophage ligases one of which clustered with the NCLDV (Figure 1).


Evolution of DNA ligases of nucleo-cytoplasmic large DNA viruses of eukaryotes: a case of hidden complexity.

Yutin N, Koonin EV - Biol. Direct (2009)

A maximum-likelihood phylogenetic tree of NAD-dependent DNA ligases. The numbers indicate the statistical support (Expected-Likelihood Weights) of internal nodes. The support values are given as percentages (n = 1,000). Archaeal sequences are color-coded red, bacterial sequences green, eukaryotic sequences brown, and viral sequences blue. The NCLDV are shown in bold type. All proteins are denoted by their Genbank identification numbers (GIs). The truncated sequence of the NAD-dependent ligase of Crocodilepox virus was not used for phylogenetic analysis. Abbreviations: MSV, Melanoplus sanguinipes entomopoxvirus; AMV, Amsacta moorei entomopoxvirus; Acapo, Acanthamoeba polyphaga mimivirus; CIV, Chilo iridescent virus (Invertebrate iridescent virus 6); Aedta, Aedes taeniorhynchus iridescent virus (Invertebrate iridescent virus 3); Ralph, Ralstonia solanacearum phage RSL1; Lenar, Lentisphaera araneosa HTCC2155; Acife, Acidithiobacillus ferrooxidans ATCC 23270; Marsp, Marinobacter sp. ELB17; Desal, Desulfatibacillum alkenivorans AK-01; Desac, Desulfuromonas acetoxidans DSM 684; Natph, Natronomonas pharaonis DSM 2160; Halwa, Haloquadratum walsbyi DSM 16790; Ostlu, Ostreococcus lucimarinus CCE9901; Ricfe, Rickettsia felis URRWXCal2; Metin, Methylacidiphilum infernorum V4; Nitsp, Nitratiruptor sp. SB155-2; Aquae, Aquifex aeolicus VF5; CanBl, Candidatus Blochmannia floridanus; Brahy, Brachyspira hyodysenteriae WA1; Lepbu, Leptotrichia buccalis DSM 1135; Dicdi, Dictyostelium discoideum AX4; Borhe, Borrelia hermsii DAH; Bacth, Bacillus thuringiensis Bt407; Cloca, Clostridium carboxidivorans P7; Plepa, Plesiocystis pacifica SIR-1; Sorce, Sorangium cellulosum.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2806865&req=5

Figure 1: A maximum-likelihood phylogenetic tree of NAD-dependent DNA ligases. The numbers indicate the statistical support (Expected-Likelihood Weights) of internal nodes. The support values are given as percentages (n = 1,000). Archaeal sequences are color-coded red, bacterial sequences green, eukaryotic sequences brown, and viral sequences blue. The NCLDV are shown in bold type. All proteins are denoted by their Genbank identification numbers (GIs). The truncated sequence of the NAD-dependent ligase of Crocodilepox virus was not used for phylogenetic analysis. Abbreviations: MSV, Melanoplus sanguinipes entomopoxvirus; AMV, Amsacta moorei entomopoxvirus; Acapo, Acanthamoeba polyphaga mimivirus; CIV, Chilo iridescent virus (Invertebrate iridescent virus 6); Aedta, Aedes taeniorhynchus iridescent virus (Invertebrate iridescent virus 3); Ralph, Ralstonia solanacearum phage RSL1; Lenar, Lentisphaera araneosa HTCC2155; Acife, Acidithiobacillus ferrooxidans ATCC 23270; Marsp, Marinobacter sp. ELB17; Desal, Desulfatibacillum alkenivorans AK-01; Desac, Desulfuromonas acetoxidans DSM 684; Natph, Natronomonas pharaonis DSM 2160; Halwa, Haloquadratum walsbyi DSM 16790; Ostlu, Ostreococcus lucimarinus CCE9901; Ricfe, Rickettsia felis URRWXCal2; Metin, Methylacidiphilum infernorum V4; Nitsp, Nitratiruptor sp. SB155-2; Aquae, Aquifex aeolicus VF5; CanBl, Candidatus Blochmannia floridanus; Brahy, Brachyspira hyodysenteriae WA1; Lepbu, Leptotrichia buccalis DSM 1135; Dicdi, Dictyostelium discoideum AX4; Borhe, Borrelia hermsii DAH; Bacth, Bacillus thuringiensis Bt407; Cloca, Clostridium carboxidivorans P7; Plepa, Plesiocystis pacifica SIR-1; Sorce, Sorangium cellulosum.
Mentions: To reconstruct the evolutionary scenario for viral ligases, we used multiple alignments of the NAD-dependent and ATP-dependent ligases that included the respective protein sequences from the NCLDV, other viruses, and representative archaea, bacteria, and eukaryotes (see Additional File 1 and Additional File 2, respectively), to build maximum likelihood (ML) phylogenetic trees. The tree for the NAD-dependent ligases contains an unequivocally supported NCLDV clade (Figure 1). Statistical evaluation of alternative tree topologies using the Approximately Unbiased (AU) test [22] indicated that trees with polyphyletic NCLDV effectively could be ruled out (all these alternative topologies had zero AU values). The NCLDV clade belonged to a branch that included mostly NAD-dependent ligases from gamma-proteobacteria along with some bacteriophage ligases one of which clustered with the NCLDV (Figure 1).

Bottom Line: 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.Shpakovski, and Igor B.Zhulin.

View Article: PubMed Central - HTML - PubMed

Affiliation: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA. yutin@ncbi.nlm.nih.gov

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.

Show MeSH
Related in: MedlinePlus