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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

FSF distribution in the viral supergroup.(A) Total number of FSFs that were either shared or uniquely present in each viral subgroup. A seven-set Venn diagram makes explicit the 127 (27 – 1) combinations that are possible with seven groups. (B) Ariadne’s threads give the most parsimonious solution to encase all highly shared FSFs between different viral subgroups. Threads were inferred directly from the seven-set Venn diagram. FSFs identified by SCOP css. (C) Number of FSFs shared in each viral subgroup with every other subgroup. Pie charts are proportional to the size of the FSF repertoire in each viral subgroup.
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Figure 4: FSF distribution in the viral supergroup.(A) Total number of FSFs that were either shared or uniquely present in each viral subgroup. A seven-set Venn diagram makes explicit the 127 (27 – 1) combinations that are possible with seven groups. (B) Ariadne’s threads give the most parsimonious solution to encase all highly shared FSFs between different viral subgroups. Threads were inferred directly from the seven-set Venn diagram. FSFs identified by SCOP css. (C) Number of FSFs shared in each viral subgroup with every other subgroup. Pie charts are proportional to the size of the FSF repertoire in each viral subgroup.

Mentions: Next, we explored how the 716 viral FSFs distributed between viral replicon types (Fig. 4). Most viral FSFs were only detected in dsDNA viruses (Fig. 4A). In comparison, proteomes of the ssDNA, ssRNA, dsRNA, and retrotranscribing groups were genetically poor. Roughly, 91% (649 of 716) of the total viral FSFs were unique to a single viral subgroup, and only ~9% (67) of the total viral FSFs were shared by more than one subgroup (Fig. 4A). The number of shared FSFs in each viral subgroup exceeded the number of unique FSFs, except for dsDNA and minus-ssRNA viruses. A seven-set Venn diagram made clear that each viral subgroup shared FSFs with every other subgroup (the sole exception being ssDNA and dsDNA-RT viruses) but did so sparsely (Fig. 4A, Venn diagram). The diagram shows that there was no single FSF common to all viral subgroups (Fig. 4A). However, it also revealed that the minus-ssRNA and dsDNA groups circumscribed the most widely shared FSFs (traces highlighted in the Venn diagram) (Table 4).


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

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

FSF distribution in the viral supergroup.(A) Total number of FSFs that were either shared or uniquely present in each viral subgroup. A seven-set Venn diagram makes explicit the 127 (27 – 1) combinations that are possible with seven groups. (B) Ariadne’s threads give the most parsimonious solution to encase all highly shared FSFs between different viral subgroups. Threads were inferred directly from the seven-set Venn diagram. FSFs identified by SCOP css. (C) Number of FSFs shared in each viral subgroup with every other subgroup. Pie charts are proportional to the size of the FSF repertoire in each viral subgroup.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: FSF distribution in the viral supergroup.(A) Total number of FSFs that were either shared or uniquely present in each viral subgroup. A seven-set Venn diagram makes explicit the 127 (27 – 1) combinations that are possible with seven groups. (B) Ariadne’s threads give the most parsimonious solution to encase all highly shared FSFs between different viral subgroups. Threads were inferred directly from the seven-set Venn diagram. FSFs identified by SCOP css. (C) Number of FSFs shared in each viral subgroup with every other subgroup. Pie charts are proportional to the size of the FSF repertoire in each viral subgroup.
Mentions: Next, we explored how the 716 viral FSFs distributed between viral replicon types (Fig. 4). Most viral FSFs were only detected in dsDNA viruses (Fig. 4A). In comparison, proteomes of the ssDNA, ssRNA, dsRNA, and retrotranscribing groups were genetically poor. Roughly, 91% (649 of 716) of the total viral FSFs were unique to a single viral subgroup, and only ~9% (67) of the total viral FSFs were shared by more than one subgroup (Fig. 4A). The number of shared FSFs in each viral subgroup exceeded the number of unique FSFs, except for dsDNA and minus-ssRNA viruses. A seven-set Venn diagram made clear that each viral subgroup shared FSFs with every other subgroup (the sole exception being ssDNA and dsDNA-RT viruses) but did so sparsely (Fig. 4A, Venn diagram). The diagram shows that there was no single FSF common to all viral subgroups (Fig. 4A). However, it also revealed that the minus-ssRNA and dsDNA groups circumscribed the most widely shared FSFs (traces highlighted in the Venn diagram) (Table 4).

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