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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

Spread of viral FSFs in cellular proteomes.(A) Violin plots comparing the spread (f value) of FSFs shared and not shared with viruses in archaeal, bacterial, and eukaryal proteomes. (B) Violin plots comparing the spread (f value) of FSFs shared with each viral subgroup in archaeal, bacterial, and eukaryal proteomes. Numbers on top indicate the total number of FSFs involved in each comparison. White circles in each boxplot represent group medians. Density trace is plotted symmetrically around the boxplots.
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Figure 2: Spread of viral FSFs in cellular proteomes.(A) Violin plots comparing the spread (f value) of FSFs shared and not shared with viruses in archaeal, bacterial, and eukaryal proteomes. (B) Violin plots comparing the spread (f value) of FSFs shared with each viral subgroup in archaeal, bacterial, and eukaryal proteomes. Numbers on top indicate the total number of FSFs involved in each comparison. White circles in each boxplot represent group medians. Density trace is plotted symmetrically around the boxplots.

Mentions: To infer the predominant direction of gene transfer (that is, virus to cell or cell to virus), we divided FSFs in each superkingdom into two sets: (i) those shared only with cells and (ii) those also shared with viruses. FSFs specific for each superkingdom (that is, A, B, and E Venn groups in Fig. 1A) were excluded because they represent gains unique to each superkingdom and de facto could not be subject to horizontal transfers unless they were later completely lost from the donor superkingdom. A total of 1022 FSFs were encoded by archaeal proteomes. After the exclusion of 24 Archaea-specific FSFs, 533 (52%) were shared only with Bacteria and Eukarya and 465 (45%) were also shared with viruses. Similarly, of 1535 total bacterial FSFs, 154 were Bacteria-specific, 786 (51%) were shared only with Archaea and Eukarya, and 595 (39%) were also shared with viruses. Finally, eukaryal proteomes encoded a total of 1661 FSFs, including 283 that were Eukarya-specific, 774 (47%) that were shared only with the superkingdoms Archaea and Bacteria, and 604 (36%) that were also shared with viruses. Next, we calculated a fractional (f) value to determine the spread of FSFs in the proteomes of each superkingdom (Fig. 2). The f value gives the spread of each FSF in modern proteomes and ranges from 0 (complete absence in sampled proteomes) to 1 (present in all proteomes).


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

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

Spread of viral FSFs in cellular proteomes.(A) Violin plots comparing the spread (f value) of FSFs shared and not shared with viruses in archaeal, bacterial, and eukaryal proteomes. (B) Violin plots comparing the spread (f value) of FSFs shared with each viral subgroup in archaeal, bacterial, and eukaryal proteomes. Numbers on top indicate the total number of FSFs involved in each comparison. White circles in each boxplot represent group medians. Density trace is plotted symmetrically around the boxplots.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Spread of viral FSFs in cellular proteomes.(A) Violin plots comparing the spread (f value) of FSFs shared and not shared with viruses in archaeal, bacterial, and eukaryal proteomes. (B) Violin plots comparing the spread (f value) of FSFs shared with each viral subgroup in archaeal, bacterial, and eukaryal proteomes. Numbers on top indicate the total number of FSFs involved in each comparison. White circles in each boxplot represent group medians. Density trace is plotted symmetrically around the boxplots.
Mentions: To infer the predominant direction of gene transfer (that is, virus to cell or cell to virus), we divided FSFs in each superkingdom into two sets: (i) those shared only with cells and (ii) those also shared with viruses. FSFs specific for each superkingdom (that is, A, B, and E Venn groups in Fig. 1A) were excluded because they represent gains unique to each superkingdom and de facto could not be subject to horizontal transfers unless they were later completely lost from the donor superkingdom. A total of 1022 FSFs were encoded by archaeal proteomes. After the exclusion of 24 Archaea-specific FSFs, 533 (52%) were shared only with Bacteria and Eukarya and 465 (45%) were also shared with viruses. Similarly, of 1535 total bacterial FSFs, 154 were Bacteria-specific, 786 (51%) were shared only with Archaea and Eukarya, and 595 (39%) were also shared with viruses. Finally, eukaryal proteomes encoded a total of 1661 FSFs, including 283 that were Eukarya-specific, 774 (47%) that were shared only with the superkingdoms Archaea and Bacteria, and 604 (36%) that were also shared with viruses. Next, we calculated a fractional (f) value to determine the spread of FSFs in the proteomes of each superkingdom (Fig. 2). The f value gives the spread of each FSF in modern proteomes and ranges from 0 (complete absence in sampled proteomes) to 1 (present in all proteomes).

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