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Widespread horizontal gene transfer from circular single-stranded DNA viruses to eukaryotic genomes.

Liu H, Fu Y, Li B, Yu X, Xie J, Cheng J, Ghabrial SA, Li G, Yi X, Jiang D - BMC Evol. Biol. (2011)

Bottom Line: In eukaryotes, retroviruses, which can integrate into host genome as an obligate step in their replication strategy, comprise approximately 8% of the human genome.We conclude that the replication initiation protein (Rep)-related sequences of geminiviruses, nanoviruses and circoviruses have been frequently transferred to a broad range of eukaryotic species, including plants, fungi, animals and protists.Some of the transferred viral genes were conserved and expressed, suggesting that these genes have been coopted to assume cellular functions in the host genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan 430070, Hubei Province, P R China.

ABSTRACT

Background: In addition to vertical transmission, organisms can also acquire genes from other distantly related species or from their extra-chromosomal elements (plasmids and viruses) via horizontal gene transfer (HGT). It has been suggested that phages represent substantial forces in prokaryotic evolution. In eukaryotes, retroviruses, which can integrate into host genome as an obligate step in their replication strategy, comprise approximately 8% of the human genome. Unlike retroviruses, few members of other virus families are known to transfer genes to host genomes.

Results: Here we performed a systematic search for sequences related to circular single-stranded DNA (ssDNA) viruses in publicly available eukaryotic genome databases followed by comprehensive phylogenetic analysis. We conclude that the replication initiation protein (Rep)-related sequences of geminiviruses, nanoviruses and circoviruses have been frequently transferred to a broad range of eukaryotic species, including plants, fungi, animals and protists. Some of the transferred viral genes were conserved and expressed, suggesting that these genes have been coopted to assume cellular functions in the host genomes. We also identified geminivirus-like and parvovirus-like transposable elements in genomes of fungi and lower animals, respectively, and thereby provide direct evidence that eukaryotic transposons could derive from ssDNA viruses.

Conclusions: Our discovery extends the host range of circular ssDNA viruses and sheds light on the origin and evolution of these viruses. It also suggests that ssDNA viruses act as an unforeseen source of genetic innovation in their hosts.

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Related in: MedlinePlus

Phylogeny of geminiviral Rep-like sequences from eukaryotes, known viruses, plasmids and phytoplasma. The phylogenetic tree was built using PhyML-mixtures based on a multiple sequence alignment generated using COBALT with the Constraint E-value parameter setting to 0.1. This tree was rooted with circoviruses and nanoviruses. The topology of blue asterisk marked clade was evaluated independently. Only p-values of the approximate likelihood ratios (SH-test) > 0.5 (50%) are indicated. scale bars correspond to 0.5 amino acid substitutions per site. Sequence accession numbers are given for each sequence.
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Figure 4: Phylogeny of geminiviral Rep-like sequences from eukaryotes, known viruses, plasmids and phytoplasma. The phylogenetic tree was built using PhyML-mixtures based on a multiple sequence alignment generated using COBALT with the Constraint E-value parameter setting to 0.1. This tree was rooted with circoviruses and nanoviruses. The topology of blue asterisk marked clade was evaluated independently. Only p-values of the approximate likelihood ratios (SH-test) > 0.5 (50%) are indicated. scale bars correspond to 0.5 amino acid substitutions per site. Sequence accession numbers are given for each sequence.

Mentions: We next performed a comprehensive phylogenetic analysis to determine the relationship between the endogenous virus-like sequences and known circular ssDNA viruses as well as among endogenous sequences (Figure 4 and Additional file 1: Figure S4). As shown in Additional file 1: Figure S4, all the sequences formed three large clades: geminivirus-like, nanovirus-like and circovirus-like. In each clade, the endogenous virus-like sequences generally clustered distinctly with the known viruses but did not fall into the established viral families, suggesting that these virus-like sequences may have originated from previously undescribed circular ssDNA viral lineages. An exception was the only virus-like sequence detected in opossum (Monodelphis domestica) genome, which clustered within the Circoviridae clade and was most closely related to pig circoviruses.


Widespread horizontal gene transfer from circular single-stranded DNA viruses to eukaryotic genomes.

Liu H, Fu Y, Li B, Yu X, Xie J, Cheng J, Ghabrial SA, Li G, Yi X, Jiang D - BMC Evol. Biol. (2011)

Phylogeny of geminiviral Rep-like sequences from eukaryotes, known viruses, plasmids and phytoplasma. The phylogenetic tree was built using PhyML-mixtures based on a multiple sequence alignment generated using COBALT with the Constraint E-value parameter setting to 0.1. This tree was rooted with circoviruses and nanoviruses. The topology of blue asterisk marked clade was evaluated independently. Only p-values of the approximate likelihood ratios (SH-test) > 0.5 (50%) are indicated. scale bars correspond to 0.5 amino acid substitutions per site. Sequence accession numbers are given for each sequence.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3198968&req=5

Figure 4: Phylogeny of geminiviral Rep-like sequences from eukaryotes, known viruses, plasmids and phytoplasma. The phylogenetic tree was built using PhyML-mixtures based on a multiple sequence alignment generated using COBALT with the Constraint E-value parameter setting to 0.1. This tree was rooted with circoviruses and nanoviruses. The topology of blue asterisk marked clade was evaluated independently. Only p-values of the approximate likelihood ratios (SH-test) > 0.5 (50%) are indicated. scale bars correspond to 0.5 amino acid substitutions per site. Sequence accession numbers are given for each sequence.
Mentions: We next performed a comprehensive phylogenetic analysis to determine the relationship between the endogenous virus-like sequences and known circular ssDNA viruses as well as among endogenous sequences (Figure 4 and Additional file 1: Figure S4). As shown in Additional file 1: Figure S4, all the sequences formed three large clades: geminivirus-like, nanovirus-like and circovirus-like. In each clade, the endogenous virus-like sequences generally clustered distinctly with the known viruses but did not fall into the established viral families, suggesting that these virus-like sequences may have originated from previously undescribed circular ssDNA viral lineages. An exception was the only virus-like sequence detected in opossum (Monodelphis domestica) genome, which clustered within the Circoviridae clade and was most closely related to pig circoviruses.

Bottom Line: In eukaryotes, retroviruses, which can integrate into host genome as an obligate step in their replication strategy, comprise approximately 8% of the human genome.We conclude that the replication initiation protein (Rep)-related sequences of geminiviruses, nanoviruses and circoviruses have been frequently transferred to a broad range of eukaryotic species, including plants, fungi, animals and protists.Some of the transferred viral genes were conserved and expressed, suggesting that these genes have been coopted to assume cellular functions in the host genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan 430070, Hubei Province, P R China.

ABSTRACT

Background: In addition to vertical transmission, organisms can also acquire genes from other distantly related species or from their extra-chromosomal elements (plasmids and viruses) via horizontal gene transfer (HGT). It has been suggested that phages represent substantial forces in prokaryotic evolution. In eukaryotes, retroviruses, which can integrate into host genome as an obligate step in their replication strategy, comprise approximately 8% of the human genome. Unlike retroviruses, few members of other virus families are known to transfer genes to host genomes.

Results: Here we performed a systematic search for sequences related to circular single-stranded DNA (ssDNA) viruses in publicly available eukaryotic genome databases followed by comprehensive phylogenetic analysis. We conclude that the replication initiation protein (Rep)-related sequences of geminiviruses, nanoviruses and circoviruses have been frequently transferred to a broad range of eukaryotic species, including plants, fungi, animals and protists. Some of the transferred viral genes were conserved and expressed, suggesting that these genes have been coopted to assume cellular functions in the host genomes. We also identified geminivirus-like and parvovirus-like transposable elements in genomes of fungi and lower animals, respectively, and thereby provide direct evidence that eukaryotic transposons could derive from ssDNA viruses.

Conclusions: Our discovery extends the host range of circular ssDNA viruses and sheds light on the origin and evolution of these viruses. It also suggests that ssDNA viruses act as an unforeseen source of genetic innovation in their hosts.

Show MeSH
Related in: MedlinePlus