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Identification of multiple independent horizontal gene transfers into poxviruses using a comparative genomics approach.

Bratke KA, McLysaght A - BMC Evol. Biol. (2008)

Bottom Line: We propose to use synteny conservation around the horizontally transferred gene (HTgene) to distinguish between single and multiple events.We examined the synteny conservation around twenty four pox genes that we identified, or which were reported in the literature, as candidate HTgenes.We found support for multiple independent transfers into poxviruses for five HTgenes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Smurfit Institute of Genetics, University of Dublin, Trinity College, Dublin 2, Ireland. bratkek@tcd.ie

ABSTRACT

Background: Poxviruses are important pathogens of humans, livestock and wild animals. These large dsDNA viruses have a set of core orthologs whose gene order is extremely well conserved throughout poxvirus genera. They also contain many genes with sequence and functional similarity to host genes which were probably acquired by horizontal gene transfer.Although phylogenetic trees can indicate the occurrence of horizontal gene transfer and even uncover multiple events, their use may be hampered by uncertainties in both the topology and the rooting of the tree. We propose to use synteny conservation around the horizontally transferred gene (HTgene) to distinguish between single and multiple events.

Results: Here we devise a method that incorporates comparative genomic information into the investigation of horizontal gene transfer, and we apply this method to poxvirus genomes. We examined the synteny conservation around twenty four pox genes that we identified, or which were reported in the literature, as candidate HTgenes. We found support for multiple independent transfers into poxviruses for five HTgenes. Three of these genes are known to be important for the survival of the virus in or out of the host cell and one of them increases susceptibility to some antiviral drugs.

Conclusion: In related genomes conserved synteny information can provide convincing evidence for multiple independent horizontal gene transfer events even in the absence of a robust phylogenetic tree for the HTgene.

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Related in: MedlinePlus

Model gene order comparisons for inferring the number of horizontal gene transfer events. The relative order of genes around the gene of interest is illustrated. Orthologous genes are shaded in the same color and lined up vertically. A white box indicates that the gene is present in the genome, but not at the expected (i.e., equivalent) location. Horizontal lines indicate genomic segments. Thick horizontal lines indicate that the connected genes are neighboring genes of the specified type (where gene of interest is present) or have fewer than three intervening genes of the specified type (where gene of interest is absent). Thin horizontal lines signify three to six intervening genes. Vertical lines separate discontiguous genomic regions. (A) The gene of interest is in an equivalent location in all genomes where it is found. This supports a single origin (i.e., horizontal transfer) of this gene. (B) The gene of interest is found in two different genomic locations and the relative arrangement of other genes in each of these locations is conserved (i.e., there is no support for a local rearrangement). This supports two independent transfers of this gene. (C) The gene of interest is found in two different genomic locations but these regions are not conserved between genomes, so it is not possible to infer if it was a single transfer followed by genome rearrangement, or two independent transfer events.
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Figure 2: Model gene order comparisons for inferring the number of horizontal gene transfer events. The relative order of genes around the gene of interest is illustrated. Orthologous genes are shaded in the same color and lined up vertically. A white box indicates that the gene is present in the genome, but not at the expected (i.e., equivalent) location. Horizontal lines indicate genomic segments. Thick horizontal lines indicate that the connected genes are neighboring genes of the specified type (where gene of interest is present) or have fewer than three intervening genes of the specified type (where gene of interest is absent). Thin horizontal lines signify three to six intervening genes. Vertical lines separate discontiguous genomic regions. (A) The gene of interest is in an equivalent location in all genomes where it is found. This supports a single origin (i.e., horizontal transfer) of this gene. (B) The gene of interest is found in two different genomic locations and the relative arrangement of other genes in each of these locations is conserved (i.e., there is no support for a local rearrangement). This supports two independent transfers of this gene. (C) The gene of interest is found in two different genomic locations but these regions are not conserved between genomes, so it is not possible to infer if it was a single transfer followed by genome rearrangement, or two independent transfer events.

Mentions: This conservation permits the comparison of the genomic location of HTgenes between genomes. Shared genomic context may also be useful for distinguishing orthologs and paralogs in conjunction with phylogenetic trees, though that analysis is not conducted here. These comparisons of HTgene locations are done with respect to gene families which are shared between the genomes of interest. Depending on the extent of gene order conservation around the HTgene between genomes it may be possible to distinguish single from multiple transfer events (Fig. 2A and 2B). If the local gene order is not well conserved then a single transfer followed by genome rearrangement cannot be excluded even when the HTgene is present in a completely different context in different genomes (Fig. 2C). Within poxvirus genera this is a particular issue when comparing EPV gene order to that of ChPV, and to a certain degree also in comparison of avipox to other ChPV because of the high amount of rearrangement (Additional File 1).


Identification of multiple independent horizontal gene transfers into poxviruses using a comparative genomics approach.

Bratke KA, McLysaght A - BMC Evol. Biol. (2008)

Model gene order comparisons for inferring the number of horizontal gene transfer events. The relative order of genes around the gene of interest is illustrated. Orthologous genes are shaded in the same color and lined up vertically. A white box indicates that the gene is present in the genome, but not at the expected (i.e., equivalent) location. Horizontal lines indicate genomic segments. Thick horizontal lines indicate that the connected genes are neighboring genes of the specified type (where gene of interest is present) or have fewer than three intervening genes of the specified type (where gene of interest is absent). Thin horizontal lines signify three to six intervening genes. Vertical lines separate discontiguous genomic regions. (A) The gene of interest is in an equivalent location in all genomes where it is found. This supports a single origin (i.e., horizontal transfer) of this gene. (B) The gene of interest is found in two different genomic locations and the relative arrangement of other genes in each of these locations is conserved (i.e., there is no support for a local rearrangement). This supports two independent transfers of this gene. (C) The gene of interest is found in two different genomic locations but these regions are not conserved between genomes, so it is not possible to infer if it was a single transfer followed by genome rearrangement, or two independent transfer events.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2268676&req=5

Figure 2: Model gene order comparisons for inferring the number of horizontal gene transfer events. The relative order of genes around the gene of interest is illustrated. Orthologous genes are shaded in the same color and lined up vertically. A white box indicates that the gene is present in the genome, but not at the expected (i.e., equivalent) location. Horizontal lines indicate genomic segments. Thick horizontal lines indicate that the connected genes are neighboring genes of the specified type (where gene of interest is present) or have fewer than three intervening genes of the specified type (where gene of interest is absent). Thin horizontal lines signify three to six intervening genes. Vertical lines separate discontiguous genomic regions. (A) The gene of interest is in an equivalent location in all genomes where it is found. This supports a single origin (i.e., horizontal transfer) of this gene. (B) The gene of interest is found in two different genomic locations and the relative arrangement of other genes in each of these locations is conserved (i.e., there is no support for a local rearrangement). This supports two independent transfers of this gene. (C) The gene of interest is found in two different genomic locations but these regions are not conserved between genomes, so it is not possible to infer if it was a single transfer followed by genome rearrangement, or two independent transfer events.
Mentions: This conservation permits the comparison of the genomic location of HTgenes between genomes. Shared genomic context may also be useful for distinguishing orthologs and paralogs in conjunction with phylogenetic trees, though that analysis is not conducted here. These comparisons of HTgene locations are done with respect to gene families which are shared between the genomes of interest. Depending on the extent of gene order conservation around the HTgene between genomes it may be possible to distinguish single from multiple transfer events (Fig. 2A and 2B). If the local gene order is not well conserved then a single transfer followed by genome rearrangement cannot be excluded even when the HTgene is present in a completely different context in different genomes (Fig. 2C). Within poxvirus genera this is a particular issue when comparing EPV gene order to that of ChPV, and to a certain degree also in comparison of avipox to other ChPV because of the high amount of rearrangement (Additional File 1).

Bottom Line: We propose to use synteny conservation around the horizontally transferred gene (HTgene) to distinguish between single and multiple events.We examined the synteny conservation around twenty four pox genes that we identified, or which were reported in the literature, as candidate HTgenes.We found support for multiple independent transfers into poxviruses for five HTgenes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Smurfit Institute of Genetics, University of Dublin, Trinity College, Dublin 2, Ireland. bratkek@tcd.ie

ABSTRACT

Background: Poxviruses are important pathogens of humans, livestock and wild animals. These large dsDNA viruses have a set of core orthologs whose gene order is extremely well conserved throughout poxvirus genera. They also contain many genes with sequence and functional similarity to host genes which were probably acquired by horizontal gene transfer.Although phylogenetic trees can indicate the occurrence of horizontal gene transfer and even uncover multiple events, their use may be hampered by uncertainties in both the topology and the rooting of the tree. We propose to use synteny conservation around the horizontally transferred gene (HTgene) to distinguish between single and multiple events.

Results: Here we devise a method that incorporates comparative genomic information into the investigation of horizontal gene transfer, and we apply this method to poxvirus genomes. We examined the synteny conservation around twenty four pox genes that we identified, or which were reported in the literature, as candidate HTgenes. We found support for multiple independent transfers into poxviruses for five HTgenes. Three of these genes are known to be important for the survival of the virus in or out of the host cell and one of them increases susceptibility to some antiviral drugs.

Conclusion: In related genomes conserved synteny information can provide convincing evidence for multiple independent horizontal gene transfer events even in the absence of a robust phylogenetic tree for the HTgene.

Show MeSH
Related in: MedlinePlus