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Hidden Evolutionary Complexity of Nucleo-Cytoplasmic Large DNA Viruses of Eukaryotes

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Hidden Evolutionary Complexity of Nucleo-Cytoplasmic Large DNA Viruses of Eukaryotes

Natalya Yutin et al. Virol J.

Abstract

Background: The Nucleo-Cytoplasmic Large DNA Viruses (NCLDV) constitute an apparently monophyletic group that consists of at least 6 families of viruses infecting a broad variety of eukaryotic hosts. A comprehensive genome comparison and maximum-likelihood reconstruction of the NCLDV evolution revealed a set of approximately 50 conserved, core genes that could be mapped to the genome of the common ancestor of this class of eukaryotic viruses.

Results: We performed a detailed phylogenetic analysis of these core NCLDV genes and applied the constrained tree approach to show that the majority of the core genes are unlikely to be monophyletic. Several of the core genes have been independently acquired from different sources by different NCLDV lineages whereas for the majority of these genes displacement by homologs from cellular organisms in one or more groups of the NCLDV was demonstrated.

Conclusions: A detailed study of the evolution of the genomic core of the NCLDV reveals substantial complexity and diversity of evolutionary scenarios that was largely unsuspected previously. The phylogenetic coherence between the core genes is sufficient to validate the hypothesis on the evolution of all NCLDV from a common ancestral virus although the set of ancestral genes might be smaller than previously inferred from patterns of gene presence-absence.

Figures

Figure 1
Figure 1
Phylogenetic trees of ancestral NCLDV genes involved in DNA replication. (A). DNA polymerase, the original ML tree. (B). DNA polymerase, constrained tree, monophyly of NCLDV, baculoviruses and herpesviruses enforced. (C). Primase-helicase. (D). FLAP endonuclease. Branches with bootstrap support less than 50 were collapsed. For each sequence, the species name abbreviation and the gene identification numbers are indicated. Species abbreviations: Arath, Arabidopsis thaliana; Desps, Desulfotalea psychrophila LSv54; Dessa, Desulfovibrio salexigens DSM 2638; Emihu, Emiliania huxleyi virus 86; Enccu, Encephalitozoon cuniculi GB-M1; Entdi, Entamoeba dispar SAW760; Lacre, Lactobacillus reuteri DSM 20016; Leibr, Leishmania braziliensis MHOM/BR/75/M2904; Macmu, Macaca mulatta; Phatr, Phaeodactylum tricornutum CCAP 1055/1; Tetth, Tetrahymena thermophila; Triva, Trichomonas vaginalis G3; Bf, Firmicutes; Bp, Proteobacteria; E8, Stramenopiles; E9, Viridiplantae; Ea, Amoebozoa; Ec, Alveolata; Ek, Euglenozoa; El, Opisthokonta; Ew, Parabasalidea; q2, Coccolithovirus.
Figure 2
Figure 2
Phylogenetic trees of ancestral NCLDV genes involved in DNA replication, recombination and repair. (A). Topoisomerase IB. (B). DNA Topoisomerase II. (C). AP endonuclease 2. (D). Nucleotidyltransferase. (E). YqaJ-like recombinase. Branches with bootstrap support less than 50 were collapsed. For each sequence, the species name abbreviation and the gene identification numbers are indicated; env stands for sequences retrieved from env_nr database. Species abbreviations: Invir, Invertebrate iridescent virus; Crovi, Crocodilepox virus; Afrsw, African swine fever virus; Amsmo, Amsacta moorei entomopoxvirus 'L'; Arath, Arabidopsis thaliana; Ectsi, Ectocarpus siliculosus virus 1; Emihu, Emiliania huxleyi virus 86; Ostlu, Ostreococcus lucimarinus CCE9901; Ostta, Ostreococcus tauri virus 1; Ostvi, Ostreococcus virus OsV5; Parbu, Paramecium bursaria Chlorella virus FR483; Phypa, Physcomitrella patens subsp. patens; Melsa, Melanoplus sanguinipes entomopoxvirus; Micsp, Micromonas sp. RCC299; Nitma, Nitrosopumilus maritimus SCM1; Ruesp, Ruegeria sp. TM1040; Sorbi, Sorghum bicolor; At, Thaumarchaeota; Bp, Proteobacteria; E9, Viridiplantae; c1, Asfarviridae; l1, Chloriridovirus; l2, Iridovirus; q1, Chlorovirus; q2, Coccolithovirus; q3, Phaeovirus; q6, unclassified Phycodnaviridae; u1, Chordopoxvirinae; u2, Entomopoxvirinae.
Figure 3
Figure 3
Phylogenetic trees of ancestral NCLDV genes involved in transcription. (A). RNA polymerase alpha subunit. (B). RNA polymerase beta subunit. (C). RNA polymerase alpha subunit, constrained tree with an NCLDV clade excluding mimivirus and ASFV. (D). Transcription factor TFIIB. Branches with bootstrap support less than 50 were collapsed. For each sequence, the species name abbreviation and the gene identification numbers are indicated; env stands for sequences retrieved from env_nr database. Species abbreviations: Acatu, Acanthocystis turfacea Chlorella virus 1; Afrsw, African swine fever virus; Emihu, Emiliania huxleyi virus 86; Hydma, Hydra magnipapillata; Ostvi, Ostreococcus virus OsV5; Parbu, Paramecium bursaria Chlorella virus FR483; ParNY, Paramecium bursaria Chlorella virus NY2A; Psyto, Psychroflexus torquis ATCC 700755; Bb, Bacteroidetes; El, Opisthokonta; c1, Asfarviridae; q1, Chlorovirus; q2, Coccolithovirus; q6, unclassified Phycodnaviridae.
Figure 4
Figure 4
Phylogenetic trees of ancestral NCLDV genes involved in mRNA processing/maturation. (A). Superfamily 2 helicases homologous to Vaccinia A18. (B). Superfamily 2 helicases homologous to Vaccinia D6 and D11. (C). Capping enzyme (guanylyltransferase domain). (D). Capping enzyme (methyltransferase domain). (E). RNA ligase. Branches with bootstrap support less than 50 were collapsed. For each sequence, the species name abbreviation and the gene identification numbers are indicated; env stands for sequences retrieved from env_nr database. Species abbreviations: Phypa, Physcomitrella patens subsp. patens; Dicdi, Dictyostelium discoideum AX4; Entdi, Entamoeba dispar SAW760; Plavi, Plasmodium vivax SaI-1; Leiin, Leishmania infantum JPCM5; Trycr, Trypanosoma cruzi strain CL Brener; Anoga, Anopheles gambiae str. PEST; Bruma, Brugia malayi; Caeel, Caenorhabditis elegans; Enccu, Encephalitozoon cuniculi GB-M1; Entbi, Enterocytozoon bieneusi H348; Monbr, Monosiga brevicollis MX1; Phano, Phaeosphaeria nodorum SN15; Strpu, Strongylocentrotus purpuratus; Trica, Tribolium castaneum; Trini, Trichoplusia ni ascovirus 2c; Afrsw, African swine fever virus; Infsp, Infectious spleen and kidney necrosis virus; Acatu, Acanthocystis turfacea Chlorella virus 1; Parbu, Paramecium bursaria Chlorella virus FR483; Emihu, Emiliania huxleyi virus 86; Ectsi, Ectocarpus siliculosus virus 1; Ostvi, Ostreococcus virus OsV5; E9, Viridiplantae; Ea, Amoebozoa; Ec, Alveolata; Ek, Euglenozoa; El, Opisthokonta; c1, Asfarviridae; l4, Megalocytivirus; q1, Chlorovirus; q2, Coccolithovirus; q3, Phaeovirus; q6, unclassified Phycodnaviridae.
Figure 5
Figure 5
Phylogenetic trees of the ancestral NCLDV genes for ribonucleotide reductase subunits. (A). Ribonucleotide reductase, large subunit. (B). Ribonucleotide reductase, small subunit. Branches with bootstrap support less than 50 were collapsed. For each sequence, the species name abbreviation and the gene identification numbers are indicated; env stands for sequences retrieved from env_nr database. Species abbreviations: Acatu, Acanthocystis turfacea Chlorella virus 1; Acypi, Acyrthosiphon pisum; Aedta, Invertebrate iridescent virus 3; Afrsw, African swine fever virus; Ambti, Ambystoma tigrinum virus; Anghe, Anguillid herpesvirus 1; Canvi, Canarypox virus; Crymu, Cryptosporidium muris RN66; Cyphe, Cyprinid herpesvirus 3; Dicdi, Dictyostelium discoideum AX4; Ectsi, Ectocarpus siliculosus virus 1; Emihu, Emiliania huxleyi virus 86; Felsp, Feldmannia species virus; Frano, Francisella novicida U112; Frovi, Frog virus 3; Helze, Heliothis zea virus 1; Infsp, Infectious spleen and kidney necrosis virus; l1_Invir, Invertebrate iridescent virus 3; l2_Invir, Invertebrate iridescent virus 6; Leibr, Leishmania braziliensis MHOM/BR/75/M2904; Lodel, Lodderomyces elongisporus NRRL YB-4239; Lymch, Lymphocystis disease virus - isolate China; Lymdi, Lymphocystis disease virus 1; Musdo, Musca domestica salivary gland hypertrophy virus; Ostvi, Ostreococcus virus OsV5; Parbu, Paramecium bursaria Chlorella virus NY2A; ParFR, Paramecium bursaria Chlorella virus FR483; Parte, Paramecium tetraurelia strain d4-2; Phatr, Phaeodactylum tricornutum CCAP 1055/1; Phoda, Photobacterium damselae subsp. damselae CIP 102761; Shrwh, Shrimp white spot syndrome virus; Singr, Singapore grouper iridovirus; Thaps, Thalassiosira pseudonana CCMP1335; Thepa, Theileria parva strain Muguga; Trybr, Trypanosoma brucei; Ustma, Ustilago maydis 521; Vibha, Vibrio harveyi 1DA3; Bp, Proteobacteria; E8, Stramenopiles; Ea, Amoebozoa; Ec, Alveolata; Ek, Euglenozoa; El, Opisthokonta; c1, Asfarviridae; k1, Herpesvirales; l1, Chloriridovirus; l2, Iridovirus; l3, Lymphocystivirus; l4, Megalocytivirus; l5, Ranavirus; o1, Nimaviridae; q1, Chlorovirus; q2, Coccolithovirus; q3, Phaeovirus; q6, unclassified Phycodnaviridae; u1, Chordopoxvirinae; vi, Nudivirus; z3, unclassified dsDNA viruses.
Figure 6
Figure 6
Phylogenetic trees of ancestral NCLDV genes encoding enzymes of nucleotide metabolism. (A). Thymidine kinase. (B). Thymidylate kinase. (C). dUTPase. Branches with bootstrap support less than 50 were collapsed. For each sequence, the species name abbreviation and the gene identification numbers are indicated; env stands for sequences retrieved from env_nr database. Species abbreviations: Acatu, Acanthocystis turfacea Chlorella virus 1; Afrsw, African swine fever virus; Agrse, Agrotis segetum granulovirus; Ambti, Ambystoma tigrinum virus; Amsmo, Amsacta moorei entomopoxvirus 'L'; Apime, Apis mellifera; Arath, Arabidopsis thaliana; Brafl, Branchiostoma floridae; Caebr, Caenorhabditis briggsae; Caeel, Caenorhabditis elegans; Canvi, Canarypox virus; Chipi, Chitinophaga pinensis DSM 2588; Cioin, Ciona intestinalis; Clobo, Clostridium botulinum A2 str. Kyoto; Cryne, Cryptococcus neoformans var. neoformans JEC21; Desha, Desulfitobacterium hafniense Y51; Dicdi, Dictyostelium discoideum AX4; Ectvi, Ectromelia virus; Emihu, Emiliania huxleyi virus 86; Enthi, Entamoeba histolytica HM-1:IMSS; Fowad, Fowl adenovirus A; Fowvi, Fowlpox virus; Frovi, Frog virus 3; Helze, Heliothis zea virus 1; Homsa, Homo sapiens; Icthe, Ictalurid herpesvirus 1; Infsp, Infectious spleen and kidney necrosis virus; l2_Invir, Invertebrate iridescent virus 6; Lacth, Lachancea thermotolerans; Leima, Leishmania major; Musdo, Musca domestica salivary gland hypertrophy virus; Nasvi, Nasonia vitripennis; Ostlu, Ostreococcus lucimarinus CCE9901; Ostta, Ostreococcus tauri virus 1; Ostvi, Ostreococcus virus OsV5; Parbu, Paramecium bursaria Chlorella virus NY2A; Parte, Paramecium tetraurelia strain d4-2; Phypa, Physcomitrella patens subsp. patens; Psesy, Pseudomonas syringae pv. syringae FF5; Rhosp, Rhodobacter sphaeroides ATCC 17025; Shrwh, Shrimp white spot syndrome virus; Singr, Singapore grouper iridovirus; Spoli, Spodoptera litura granulovirus; Tetth, Tetrahymena thermophila; Trybr, Trypanosoma brucei; Vacvi, Vaccinia virus; Varvi, Variola virus; Bb, Bacteroidetes; Bf, Firmicutes; Bp, Proteobacteria; E9, Viridiplantae; Ea, Amoebozoa; Ec, Alveolata; Ek, Euglenozoa; El, Opisthokonta; a2, Adenoviridae; c1, Asfarviridae; d2, Baculoviridae; k1, Herpesvirales; l2, Iridovirus; l4, Megalocytivirus; l5, Ranavirus; o1, Nimaviridae; q1, Chlorovirus; q2, Coccolithovirus; q6, unclassified Phycodnaviridae; u1, Chordopoxvirinae; u2, Entomopoxvirinae; vi, Nudivirus; z3, unclassified dsDNA viruses.
Figure 7
Figure 7
Phylogenetic tree of an ancestral NCLDV gene encoding an enzyme involved in virion morphogenesis: protein disulfide isomerase. Branches with bootstrap support less than 50 were collapsed. For each sequence, the species name abbreviation and the gene identification numbers are indicated; env stands for sequences retrieved from env_nr database. Species abbreviations: Afrsw, African swine fever virus; Aedta, Invertebrate iridescent virus 3; Invir, Invertebrate iridescent virus; ParAR, Paramecium bursaria Chlorella virus AR158; Emihu, Emiliania huxleyi virus 86; Ectsi, Ectocarpus siliculosus virus 1; Felsp, Feldmannia species virus; c1, Asfarviridae; l1, Chloriridovirus; l2, Iridovirus; q1, Chlorovirus; q2, Coccolithovirus; q3, Phaeovirus.

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References

    1. Forterre P. The origin of viruses and their possible roles in major evolutionary transitions. Virus Res. 2006;117(1):5–16. - PubMed
    1. Koonin EV, Senkevich TG, Dolja VV. The ancient virus world and evolution of cells. Biol Direct. 2006;1(1):29. - PMC - PubMed
    1. Iyer LM, Aravind L, Koonin EV. Common origin of four diverse families of large eukaryotic DNA viruses. J Virol. 2001;75(23):11720–11734. - PMC - PubMed
    1. Iyer LM, Balaji S, Koonin EV, Aravind L. Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res. 2006;117(1):156–184. - PubMed
    1. Yutin N, Wolf YI, Raoult D, Koonin EV. Eukaryotic large nucleo-cytoplasmic DNA viruses: clusters of orthologous genes and reconstruction of viral genome evolution. Virol J. 2009;6:223. - PMC - PubMed

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