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. 2012 Jun 11:7:13.
doi: 10.1186/1745-6150-7-13.

A novel virus genome discovered in an extreme environment suggests recombination between unrelated groups of RNA and DNA viruses

Geoffrey S Diemer  1 , Kenneth M Stedman
Affiliations

A novel virus genome discovered in an extreme environment suggests recombination between unrelated groups of RNA and DNA viruses

Geoffrey S Diemer et al. Biol Direct. .

Abstract

Background: Viruses are known to be the most abundant organisms on earth, yet little is known about their collective origin and evolutionary history. With exceptionally high rates of genetic mutation and mosaicism, it is not currently possible to resolve deep evolutionary histories of the known major virus groups. Metagenomics offers a potential means of establishing a more comprehensive view of viral evolution as vast amounts of new sequence data becomes available for comparative analysis.

Results: Bioinformatic analysis of viral metagenomic sequences derived from a hot, acidic lake revealed a circular, putatively single-stranded DNA virus encoding a major capsid protein similar to those found only in single-stranded RNA viruses. The presence and circular configuration of the complete virus genome was confirmed by inverse PCR amplification from native DNA extracted from lake sediment. The virus genome appears to be the result of a RNA-DNA recombination event between two ostensibly unrelated virus groups. Environmental sequence databases were examined for homologous genes arranged in similar configurations and three similar putative virus genomes from marine environments were identified. This result indicates the existence of a widespread but previously undetected group of viruses.

Conclusions: This unique viral genome carries implications for theories of virus emergence and evolution, as no mechanism for interviral RNA-DNA recombination has yet been identified, and only scant evidence exists that genetic exchange occurs between such distinct virus lineages.

Reviewers: This article was reviewed by EK, MK (nominated by PF) and AM. For the full reviews, please go to the Reviewers' comments section.

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Figures

Figure 1
Figure 1
Organiztion of the BSL RDHV genome.(A)Schematic representations of tombusvirus, BSL RDHV and porcine circovirus (PCV) genomes: Tombusviruses are linear ssRNA viruses, BSL RDHV and PCV are circular ssDNA viruses. Bars below ORFs indicate protein families detected by InterProScan. (B) Comparison of PCV-1 and BSL RDHV stem-loops: Both BSL RDHV and circoviruses have a conserved stem-loop in the intergenic region upstream of Rep. Black text indicates sequence identity. Nonanucleotide replication origins in the 13nt loop are boxed. Brackets indicate the 9 nucleotide stem preceding hexamer repeats H1 and H2 (gray boxes).
Figure 2
Figure 2
BLASTp data for Rep amino acid sequences. The BSL RDHV Rep ORF amino acid sequence was compared to related Rep sequences using BLASTp. Output parameters are shown. Virus family designations are indicated when possible. (GOS) Global Ocean Survey paired-end read scaffolds 10666 and 6801. (PCV2) Porcine Circovirus-2, (StCV) Starling Circovirus, (DfCyV) Dragonfly Cyclovirus. (BBTV) Banana Bunchy Top Virus, (SCSV) Subterranean Clover Stunt Virus. (TPCTV) Tomato Pseudo Curly Top Virus, (HrCTV) Horseradish Curly Top Virus.
Figure 3
Figure 3
Rolling circle replicase (Rep) and capsid protein (CP) phylogenies.(A) The Rep protein phylogeny was inferred from 204 conserved amino acid positions using the Neighbor-Joining method. Bootstrap values above a 60% significance threshold, based on 1000 replicates, are shown next to the branches. NANOVIRIDAE: (SCSV) Subterranean Clover Stunt Virus, (BBTV) Banana Bunchy Top Virus. CIRCOVIRIDAE: (DfCyV) Dragonfly Cyclovirus, (BatCV) Bat Circovirus, (StCV) Starling Circovirus, (PCV2) Porcine Circovirus-2. (GOS) Global Ocean Survey paired-end read scaffolds 6801 and 10666. (B) The capsid protein (CP) phylogeny was inferred from 256 conserved amino acid positions using the Neighbor-Joining method. Bootstrap values above a 60% significance threshold, based on 1000 replicates, are shown next to the branches. TOMBUSVIRIDAE: Dianthoviruses; (RCNMV) Red Clover Necrotic Mosaic Virus, (CRSV) Carnation Ringspot Virus. Aureusviruses: (CLSV) Cucumber Leaf Spot Virus, (PLV) Pothos Latent Virus. Tombusviruses; (AMCV) Artichoke Mottled Crinkle Virus, (TBSV) Tomato Bushy Stunt Virus, (HaRV) Havel River Tombusvirus. Unclassified Tombusviridae; (PLPV) Pelargonium Line Pattern Virus. Carmoviruses; (MNSV) Melon Necrotic Spot Virus, (SgCV) Saguaro Cactus Virus, (CMtV) Carnation Mottle Virus, (TCV) Turnip Crinkle Virus. Avenavirus; (OCSV) Oat Chlorotic Stunt Virus. NODAVIRIDAE-like: (SmV-A) Sclerophthora macrospora Virus-A, (PhV-A) Plasmopara halstedii Virus-A. (GOS) Global Ocean Survey paired-end read sequence 10665. Virus proteins for which structures are available are listed with the Protein Data Bank (PDB) identification code after the virus abbreviation.
Figure 4
Figure 4
Rolling circle replicase (Rep) amino acid multiple sequence alignment. The BSL RDHV Rep ORF sequence (BSL_Rep_ORF) is aligned to closely related sequences retrieved from NCBI using PSI-BLAST searches. Sequence alignment was performed using ClustalW set to default parameters in MEGA v.5. The endonuclease domain motifs I, II and III, and superfamily-3 helicase domain Walker A P-loop NTPase (W-A P-loop), Walker B (W-B), B’ and C motifs are boxed and labeled. Rep nuclease (RCRE) and superfamily-3 helicase (S3H helicase) domains are indicated by block arrows above the sequence alignment. A ClustalW color scheme is applied to the multiple alignment using Jalview. The range of amino acid residues used in the alignment are shown after the sequence name. (GOS) Global Ocean Survey paired-end read scaffolds 10666 and 6801. CIRCOVIRIDAE: (PCV2) Porcine Circovirus-2, (StCV) Starling Circovirus, (BatCV) Bat Circovirus, (DfCyV) Dragonfly Cyclovirus. NANOVIRIDAE: (BBTV) Banana Bunchy Top Virus, (SCSV) Subterranean Clover Stunt Virus.
Figure 5
Figure 5
BLASTp data for capsid protein (CP) amino acid sequences. The BSL RDHV CP ORF amino acid sequence was compared to related CP sequences using BLASTp. Output parameters are shown. Virus family designations are indicated when possible. (GOS) Global Ocean Survey paired-end read sequences 10665 and 6800. (SmV-A) Sclerophthora macrospora Virus-A, (PhV-A) Plasmopara halstedii Virus-A. (HaRV) Havel River Tombusvirus, (TBSV) Tomato Bushy Stunt Virus, (OCSV) Oat Chlorotic Stunt Virus, (MNSV) Melon Necrotic Spot Virus, (SgCV) Saguaro Cactus Virus, (TCV) Turnip Crinkle Virus, (CMtV) Carnation Mottle Virus, (RCNMV) Red Clover Necrotic Mosaic Virus, (CRSV) Carnation Ringspot Virus, (STNV) Satellite of Tobacco Necrosis Virus, (SV-MWLMV) Satellite Virus of Maize White Line Mosaic Virus, (SCSV) Subterranean Clover Stunt Virus, (BBTV) Banana Bunchy Top Virus, (HrCTV) Horseradish Curly Top Virus, (PCV2) Porcine Circovirus-2, (StCV) Starling Circovirus, (DfCyV) Dragonfly Cyclovirus.
Figure 6
Figure 6
Capsid protein (CP) amino acid multiple sequence alignment. The BSL RDHV CP ORF sequence (BSL_Cap_ORF) is aligned to closely related sequences retrieved from PSI-BLAST searches using ClustalW set to default parameters in MEGA v.5. The R, a, S, h and P domain regions are indicated by block arrows above the sequence alignment. A ClustalW color scheme is applied to the multiple alignment using Jalview. (GOS) Global Ocean Survey paired-end read scaffold 10665. NODAVIRIDAE-like: (PhV-A) Plasmopara halstedii Virus-A, (SmV-A) Sclerophthora macrospora Virus-A. TOMBUSVIRIDAE: Avenavirus; (OCSV) Oat Chlorotic Stunt Virus. Carmoviruses; (MNSV) Melon Necrotic Spot Virus, (CMtV) Carnation Mottle Virus, (TCV) Turnip Crinkle Virus. Tombusvirus; (TBSV) Tomato Bushy Stunt Virus. The range of amino acid residues used in the alignment are shown after the sequence name. Virus proteins for which structures are available are listed with the Protein Data Bank (PDB) identification code after the virus abbreviation.
Figure 7
Figure 7
BSL RDHV predicted protein structures.(A)Structural analysis of the BSL RDHV capsid protein: The predicted structure for residues 156–302 of the BSL RDHV capsid protein monomer ORF is overlaid on the Tomato Bushy Stunt Virus (PDB ID: 2TBV) and Melon Necrotic Spot Virus (PDB ID: 2ZAH) capsid proteins (latter two are not shown). The predicted BSL RDHV capsid is color-coded by the “Qres” dimensional structure-fitting parameter score, by BLOSUM80, and by percent amino acid sequence identity. (B)Structural analysis of the BSL RDHV replicase catalytic core: The predicted BSL RDHV Rep nuclease domain structure (colored by Qres) threaded onto PCV2 Rep (PDB ID: 2HW0) in silver. The conserved active-site tyrosine is shown in yellow.
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