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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

Circovirus-like sequences in dog and cat genome were validated by PCR amplification and sequencing. PCR products were fractionated by gel electrophoresis on 1% agarose gels and stained with ethidium bromide. Marker, DNA marker DL 2000. The sequences of bands of the expected sizes from lanes: Chr 5, Chr 22, 071, and 274 were deposited under Genbank accession numbers: JF414126-JF414131.
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Figure 2: Circovirus-like sequences in dog and cat genome were validated by PCR amplification and sequencing. PCR products were fractionated by gel electrophoresis on 1% agarose gels and stained with ethidium bromide. Marker, DNA marker DL 2000. The sequences of bands of the expected sizes from lanes: Chr 5, Chr 22, 071, and 274 were deposited under Genbank accession numbers: JF414126-JF414131.

Mentions: Because circular ssDNA viruses replicate their genomes in the nuclei of their host cells, sequence similarities between these viruses and host genomes could be attributed to trivial contamination of eukaryotic genomic DNA with viral sequences during cloning or sequence assembly. To rule out this possibility, we did a closer inspection of the raw sequence reads used for WGS assembly and the results indicated deep sequencing coverage across the junctions between the endogenous virus-like sequences and adjacent cellular sequences (see Additional file 2: Tabular data S2). These results suggest that the endogenous viral sequences were not artifacts of cloning or sequence assembly. For some eukaryotic genomes, the trace archives were not available, but their endogenous viral sequences underwent various degrees of degradation (see Additional file 2: Tabular data S2), suggesting that the viral sequences had invaded host genomes millions of years ago and therefore represent established germline infections. To validate these observations, we amplified and sequenced the endogenous circovirus-like sequences and their flanking host sequences from dog and cat tissues (Figure 2). The results revealed that the PCR products were of the expected sizes and the experimental sequences were identical to relevant regions of sequenced animal genomes.


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)

Circovirus-like sequences in dog and cat genome were validated by PCR amplification and sequencing. PCR products were fractionated by gel electrophoresis on 1% agarose gels and stained with ethidium bromide. Marker, DNA marker DL 2000. The sequences of bands of the expected sizes from lanes: Chr 5, Chr 22, 071, and 274 were deposited under Genbank accession numbers: JF414126-JF414131.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Circovirus-like sequences in dog and cat genome were validated by PCR amplification and sequencing. PCR products were fractionated by gel electrophoresis on 1% agarose gels and stained with ethidium bromide. Marker, DNA marker DL 2000. The sequences of bands of the expected sizes from lanes: Chr 5, Chr 22, 071, and 274 were deposited under Genbank accession numbers: JF414126-JF414131.
Mentions: Because circular ssDNA viruses replicate their genomes in the nuclei of their host cells, sequence similarities between these viruses and host genomes could be attributed to trivial contamination of eukaryotic genomic DNA with viral sequences during cloning or sequence assembly. To rule out this possibility, we did a closer inspection of the raw sequence reads used for WGS assembly and the results indicated deep sequencing coverage across the junctions between the endogenous virus-like sequences and adjacent cellular sequences (see Additional file 2: Tabular data S2). These results suggest that the endogenous viral sequences were not artifacts of cloning or sequence assembly. For some eukaryotic genomes, the trace archives were not available, but their endogenous viral sequences underwent various degrees of degradation (see Additional file 2: Tabular data S2), suggesting that the viral sequences had invaded host genomes millions of years ago and therefore represent established germline infections. To validate these observations, we amplified and sequenced the endogenous circovirus-like sequences and their flanking host sequences from dog and cat tissues (Figure 2). The results revealed that the PCR products were of the expected sizes and the experimental sequences were identical to relevant regions of sequenced animal genomes.

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