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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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A tree of eukaryotes showing the known distribution of endogenous viral-like sequences and exogenous circo-, nano- and geminivirus like viruses. This tree was drawn base on The Tree of Life Web Project (http://tolweb.org/).
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Figure 7: A tree of eukaryotes showing the known distribution of endogenous viral-like sequences and exogenous circo-, nano- and geminivirus like viruses. This tree was drawn base on The Tree of Life Web Project (http://tolweb.org/).

Mentions: Altogether, we discovered endogenous ssDNA virus-like sequences in host species broadly distributed in four of the five supergroups of eukaryotes [51], namely Unikonta (including animals, fungi and Entamoeba), Plantae (including land plants and green algae), Chromalveolata (including diatoms and Blastocystis) and Excavata (including Giardia) (Figure 7). The endogenous viral sequences identified here as molecular fossil records of past viral invasions provide unambiguous definitive hosts for these viruses and extend the host range of circular ssDNA viruses.


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)

A tree of eukaryotes showing the known distribution of endogenous viral-like sequences and exogenous circo-, nano- and geminivirus like viruses. This tree was drawn base on The Tree of Life Web Project (http://tolweb.org/).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 7: A tree of eukaryotes showing the known distribution of endogenous viral-like sequences and exogenous circo-, nano- and geminivirus like viruses. This tree was drawn base on The Tree of Life Web Project (http://tolweb.org/).
Mentions: Altogether, we discovered endogenous ssDNA virus-like sequences in host species broadly distributed in four of the five supergroups of eukaryotes [51], namely Unikonta (including animals, fungi and Entamoeba), Plantae (including land plants and green algae), Chromalveolata (including diatoms and Blastocystis) and Excavata (including Giardia) (Figure 7). The endogenous viral sequences identified here as molecular fossil records of past viral invasions provide unambiguous definitive hosts for these viruses and extend the host range of circular ssDNA viruses.

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