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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

Organization and transcription maps of endogenous viral Rep-like genes. Blue arrowhead boxes indicate Rep-like ORFs. Similar regions of expressed sequences are identified and the % nt identity with endogenous viral sequences are indicated. Note that the actual endogenous viral sequence extended beyond the ORF in two contigs (AAFB02000406.1 and AAFB02000468.1) of Entamoeba histolytica.
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Figure 6: Organization and transcription maps of endogenous viral Rep-like genes. Blue arrowhead boxes indicate Rep-like ORFs. Similar regions of expressed sequences are identified and the % nt identity with endogenous viral sequences are indicated. Note that the actual endogenous viral sequence extended beyond the ORF in two contigs (AAFB02000406.1 and AAFB02000468.1) of Entamoeba histolytica.

Mentions: Examination of the potential coding capacity of endogenous viral sequences indicates that most were truncated and degraded, containing numerous premature stop codons, frameshift mutations, and insertions or deletions (see Additional file 2: Tabular data S2), suggesting that these are unlikely to have functions. Some endogenous viral sequences however, were found to encode uninterrupted ORFs. The conservation of relatively long ORFs suggests that they may have evolved under functional constraints since integration. While intact ORFs could also reflect recent insertion rather than functional maintenance in a long-standing history within the host genome. Analysis of transcription products can provide stronger evidence of functional maintenance. Accordingly, we used putative amino acid sequences of endogenous viral sequences to search NCBI Expressed Sequence Tags (ESTs) database for the corresponding mRNAs with the tBLASTn program. Through subsequent sequence comparisons, it was clear that some endogenous viral sequences are expressed as mRNAs in host genomes because they share high sequence identity with most of their ESTs and adjacent host sequences over full-length sequences (Figure 6 and Additional file 2: Tabular data S4). Interestingly, ESTs related to endogenous viral sequences of the rice blast fungus M. oryzae and two roundworm species were found in related species whose genome sequences are not currently available, suggesting that there were similarly expressed insertions in these species. In fact, we have also amplified these virus-like sequences from different strains of the rice blast fungus and detected their expression (data not shown).


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)

Organization and transcription maps of endogenous viral Rep-like genes. Blue arrowhead boxes indicate Rep-like ORFs. Similar regions of expressed sequences are identified and the % nt identity with endogenous viral sequences are indicated. Note that the actual endogenous viral sequence extended beyond the ORF in two contigs (AAFB02000406.1 and AAFB02000468.1) of Entamoeba histolytica.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: Organization and transcription maps of endogenous viral Rep-like genes. Blue arrowhead boxes indicate Rep-like ORFs. Similar regions of expressed sequences are identified and the % nt identity with endogenous viral sequences are indicated. Note that the actual endogenous viral sequence extended beyond the ORF in two contigs (AAFB02000406.1 and AAFB02000468.1) of Entamoeba histolytica.
Mentions: Examination of the potential coding capacity of endogenous viral sequences indicates that most were truncated and degraded, containing numerous premature stop codons, frameshift mutations, and insertions or deletions (see Additional file 2: Tabular data S2), suggesting that these are unlikely to have functions. Some endogenous viral sequences however, were found to encode uninterrupted ORFs. The conservation of relatively long ORFs suggests that they may have evolved under functional constraints since integration. While intact ORFs could also reflect recent insertion rather than functional maintenance in a long-standing history within the host genome. Analysis of transcription products can provide stronger evidence of functional maintenance. Accordingly, we used putative amino acid sequences of endogenous viral sequences to search NCBI Expressed Sequence Tags (ESTs) database for the corresponding mRNAs with the tBLASTn program. Through subsequent sequence comparisons, it was clear that some endogenous viral sequences are expressed as mRNAs in host genomes because they share high sequence identity with most of their ESTs and adjacent host sequences over full-length sequences (Figure 6 and Additional file 2: Tabular data S4). Interestingly, ESTs related to endogenous viral sequences of the rice blast fungus M. oryzae and two roundworm species were found in related species whose genome sequences are not currently available, suggesting that there were similarly expressed insertions in these species. In fact, we have also amplified these virus-like sequences from different strains of the rice blast fungus and detected their expression (data not shown).

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