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A phylogenomic data-driven exploration of viral origins and evolution.

Nasir A, Caetano-Anollés G - Sci Adv (2015)

Bottom Line: Although numerous hypotheses have attempted to explain viral origins, none is backed by substantive data.Despite the extremely reduced nature of viral proteomes, we established an ancient origin of the "viral supergroup" and the existence of widespread episodes of horizontal transfer of genetic information.Phylogenomic analysis uncovered a universal tree of life and revealed that modern viruses reduced from multiple ancient cells that harbored segmented RNA genomes and coexisted with the ancestors of modern cells.

View Article: PubMed Central - PubMed

Affiliation: Evolutionary Bioinformatics Laboratory, Department of Crop Sciences and Illinois Informatics Institute, University of Illinois, Urbana, IL 61801, USA.

ABSTRACT
The origin of viruses remains mysterious because of their diverse and patchy molecular and functional makeup. Although numerous hypotheses have attempted to explain viral origins, none is backed by substantive data. We take full advantage of the wealth of available protein structural and functional data to explore the evolution of the proteomic makeup of thousands of cells and viruses. Despite the extremely reduced nature of viral proteomes, we established an ancient origin of the "viral supergroup" and the existence of widespread episodes of horizontal transfer of genetic information. Viruses harboring different replicon types and infecting distantly related hosts shared many metabolic and informational protein structural domains of ancient origin that were also widespread in cellular proteomes. Phylogenomic analysis uncovered a universal tree of life and revealed that modern viruses reduced from multiple ancient cells that harbored segmented RNA genomes and coexisted with the ancestors of modern cells. The model for the origin and evolution of viruses and cells is backed by strong genomic and structural evidence and can be reconciled with existing models of viral evolution if one considers viruses to have originated from ancient cells and not from modern counterparts.

No MeSH data available.


Related in: MedlinePlus

Evolutionary relationships between cells and viruses.(A) ToP describing the evolution of 368 proteomes (taxa) that were randomly sampled from cells and viruses and were distinguished by the abundance of 442 ABEV FSFs (characters) (tree length = 45,935; retention index = 0.83; g1 = −0.31). All characters were parsimony informative. Differently colored branches represent BS support values. Major groups are identified. Viral genera names are given inside parentheses. The viral order “Megavirales” is awaiting approval by the ICTV and hence written inside quotes. Viral families that form largely unified or monophyletic groups are labeled with an asterisk. Virion morphotypes were mapped to ToP and illustrated with images from the ViralZone Web resource (131). No picture was available for Turriviridae. aActinobacteria, Bacteroidetes/Chlorobi, Chloroflexi, Cyanobacteria, Fibrobacter, Firmicutes, Planctomycetes, and Thermotogae. (B) A distance-based phylogenomic network reconstructed from the occurrence of 442 ABEV FSFs in randomly sampled 368 proteomes (uncorrected P distance; equal angle; least-squares fit = 99.46). Numbers on branches indicate BS support values. Taxa were colored for easy visualization. Important groups are labeled. bActinobacteria, Bacteroidetes/Chlorobi, Chloroflexi, Cyanobacteria, Deinococcus-Thermus, Fibrobacter, Firmicutes, and Planctomycetes. cAmoebozoa and Chromalveolata.
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Figure 7: Evolutionary relationships between cells and viruses.(A) ToP describing the evolution of 368 proteomes (taxa) that were randomly sampled from cells and viruses and were distinguished by the abundance of 442 ABEV FSFs (characters) (tree length = 45,935; retention index = 0.83; g1 = −0.31). All characters were parsimony informative. Differently colored branches represent BS support values. Major groups are identified. Viral genera names are given inside parentheses. The viral order “Megavirales” is awaiting approval by the ICTV and hence written inside quotes. Viral families that form largely unified or monophyletic groups are labeled with an asterisk. Virion morphotypes were mapped to ToP and illustrated with images from the ViralZone Web resource (131). No picture was available for Turriviridae. aActinobacteria, Bacteroidetes/Chlorobi, Chloroflexi, Cyanobacteria, Fibrobacter, Firmicutes, Planctomycetes, and Thermotogae. (B) A distance-based phylogenomic network reconstructed from the occurrence of 442 ABEV FSFs in randomly sampled 368 proteomes (uncorrected P distance; equal angle; least-squares fit = 99.46). Numbers on branches indicate BS support values. Taxa were colored for easy visualization. Important groups are labeled. bActinobacteria, Bacteroidetes/Chlorobi, Chloroflexi, Cyanobacteria, Deinococcus-Thermus, Fibrobacter, Firmicutes, and Planctomycetes. cAmoebozoa and Chromalveolata.

Mentions: (iii) Evidence from trees of proteomes (ToP). To describe the evolutionary relationships between the proteomes of cells and the proteomes of viruses (taxa), we reconstructed ToP from the abundance and occurrence of 442 ABEV FSFs (phylogenetic characters). The ABEV group was selected because it includes many FSFs of ancient origin (median nd ~0.4; Fig. 5A), the entire abe core (Fig. 3B and table S5), and ancient FSFs in Ariadne’s threads (Figs. 4B and 6A). Because biases in taxon sampling could influence tree reconstruction, we randomly sampled a set of 368 proteomes (taxa) from cells and viruses, including up to 5 viral species from each viral order or family and 34 proteomes corresponding to only free-living organisms in Archaea, Bacteria, and Eukarya. The rooted phylogeny dissected proteomes into four supergroups (Fig. 7A). Viruses formed a distinct paraphyletic group at the base of ToP that was distinguishable from cells by 76% bootstrap (BS) support. In turn, archaeal organisms were clustered paraphyletically in the more basal branches (black circles), whereas Bacteria and Eukarya formed monophyletic groups (blue and green circles) supported by 66% and 100% BS, respectively (Fig. 7A). This topology supported an ancient origin of both viruses and Archaea and a sister relationship between Bacteria and Eukarya, which goes against some gene sequence–based phylogenies (58–60) but is congruent with a number of structure- and function-based studies [discussed elsewhere (18, 61–65)].


A phylogenomic data-driven exploration of viral origins and evolution.

Nasir A, Caetano-Anollés G - Sci Adv (2015)

Evolutionary relationships between cells and viruses.(A) ToP describing the evolution of 368 proteomes (taxa) that were randomly sampled from cells and viruses and were distinguished by the abundance of 442 ABEV FSFs (characters) (tree length = 45,935; retention index = 0.83; g1 = −0.31). All characters were parsimony informative. Differently colored branches represent BS support values. Major groups are identified. Viral genera names are given inside parentheses. The viral order “Megavirales” is awaiting approval by the ICTV and hence written inside quotes. Viral families that form largely unified or monophyletic groups are labeled with an asterisk. Virion morphotypes were mapped to ToP and illustrated with images from the ViralZone Web resource (131). No picture was available for Turriviridae. aActinobacteria, Bacteroidetes/Chlorobi, Chloroflexi, Cyanobacteria, Fibrobacter, Firmicutes, Planctomycetes, and Thermotogae. (B) A distance-based phylogenomic network reconstructed from the occurrence of 442 ABEV FSFs in randomly sampled 368 proteomes (uncorrected P distance; equal angle; least-squares fit = 99.46). Numbers on branches indicate BS support values. Taxa were colored for easy visualization. Important groups are labeled. bActinobacteria, Bacteroidetes/Chlorobi, Chloroflexi, Cyanobacteria, Deinococcus-Thermus, Fibrobacter, Firmicutes, and Planctomycetes. cAmoebozoa and Chromalveolata.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4643759&req=5

Figure 7: Evolutionary relationships between cells and viruses.(A) ToP describing the evolution of 368 proteomes (taxa) that were randomly sampled from cells and viruses and were distinguished by the abundance of 442 ABEV FSFs (characters) (tree length = 45,935; retention index = 0.83; g1 = −0.31). All characters were parsimony informative. Differently colored branches represent BS support values. Major groups are identified. Viral genera names are given inside parentheses. The viral order “Megavirales” is awaiting approval by the ICTV and hence written inside quotes. Viral families that form largely unified or monophyletic groups are labeled with an asterisk. Virion morphotypes were mapped to ToP and illustrated with images from the ViralZone Web resource (131). No picture was available for Turriviridae. aActinobacteria, Bacteroidetes/Chlorobi, Chloroflexi, Cyanobacteria, Fibrobacter, Firmicutes, Planctomycetes, and Thermotogae. (B) A distance-based phylogenomic network reconstructed from the occurrence of 442 ABEV FSFs in randomly sampled 368 proteomes (uncorrected P distance; equal angle; least-squares fit = 99.46). Numbers on branches indicate BS support values. Taxa were colored for easy visualization. Important groups are labeled. bActinobacteria, Bacteroidetes/Chlorobi, Chloroflexi, Cyanobacteria, Deinococcus-Thermus, Fibrobacter, Firmicutes, and Planctomycetes. cAmoebozoa and Chromalveolata.
Mentions: (iii) Evidence from trees of proteomes (ToP). To describe the evolutionary relationships between the proteomes of cells and the proteomes of viruses (taxa), we reconstructed ToP from the abundance and occurrence of 442 ABEV FSFs (phylogenetic characters). The ABEV group was selected because it includes many FSFs of ancient origin (median nd ~0.4; Fig. 5A), the entire abe core (Fig. 3B and table S5), and ancient FSFs in Ariadne’s threads (Figs. 4B and 6A). Because biases in taxon sampling could influence tree reconstruction, we randomly sampled a set of 368 proteomes (taxa) from cells and viruses, including up to 5 viral species from each viral order or family and 34 proteomes corresponding to only free-living organisms in Archaea, Bacteria, and Eukarya. The rooted phylogeny dissected proteomes into four supergroups (Fig. 7A). Viruses formed a distinct paraphyletic group at the base of ToP that was distinguishable from cells by 76% bootstrap (BS) support. In turn, archaeal organisms were clustered paraphyletically in the more basal branches (black circles), whereas Bacteria and Eukarya formed monophyletic groups (blue and green circles) supported by 66% and 100% BS, respectively (Fig. 7A). This topology supported an ancient origin of both viruses and Archaea and a sister relationship between Bacteria and Eukarya, which goes against some gene sequence–based phylogenies (58–60) but is congruent with a number of structure- and function-based studies [discussed elsewhere (18, 61–65)].

Bottom Line: Although numerous hypotheses have attempted to explain viral origins, none is backed by substantive data.Despite the extremely reduced nature of viral proteomes, we established an ancient origin of the "viral supergroup" and the existence of widespread episodes of horizontal transfer of genetic information.Phylogenomic analysis uncovered a universal tree of life and revealed that modern viruses reduced from multiple ancient cells that harbored segmented RNA genomes and coexisted with the ancestors of modern cells.

View Article: PubMed Central - PubMed

Affiliation: Evolutionary Bioinformatics Laboratory, Department of Crop Sciences and Illinois Informatics Institute, University of Illinois, Urbana, IL 61801, USA.

ABSTRACT
The origin of viruses remains mysterious because of their diverse and patchy molecular and functional makeup. Although numerous hypotheses have attempted to explain viral origins, none is backed by substantive data. We take full advantage of the wealth of available protein structural and functional data to explore the evolution of the proteomic makeup of thousands of cells and viruses. Despite the extremely reduced nature of viral proteomes, we established an ancient origin of the "viral supergroup" and the existence of widespread episodes of horizontal transfer of genetic information. Viruses harboring different replicon types and infecting distantly related hosts shared many metabolic and informational protein structural domains of ancient origin that were also widespread in cellular proteomes. Phylogenomic analysis uncovered a universal tree of life and revealed that modern viruses reduced from multiple ancient cells that harbored segmented RNA genomes and coexisted with the ancestors of modern cells. The model for the origin and evolution of viruses and cells is backed by strong genomic and structural evidence and can be reconciled with existing models of viral evolution if one considers viruses to have originated from ancient cells and not from modern counterparts.

No MeSH data available.


Related in: MedlinePlus