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Multiple genome comparison within a bacterial species reveals a unit of evolution spanning two adjacent genes in a tandem paralog cluster.

Tsuru T, Kobayashi I - Mol. Biol. Evol. (2008)

Bottom Line: A highly conserved nucleotide sequence found within every lpl ORF is likely to provide a site for homologous recombination.This result has strong impact on our understanding of gene evolution because most gene lineages underwent tandem duplication and then diversified.This work also illustrates the use of multiple genome sequences for high-resolution evolutionary analysis within the same species.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Social Genome Sciences, Department of Medical Genome Sciences, Graduate School of Frontier Sciences, University of Tokyo, Tokyo, Japan.

ABSTRACT
It has been assumed that an open reading frame (ORF) represents a unit of gene evolution as well as a unit of gene expression and function. In the present work, we report a case in which a unit comprising the 3' region of an ORF linked to a downstream intergenic region that is in turn linked to the 5' region of a downstream ORF has been conserved, and has served as the unit of gene evolution. The genes are tandem paralogous genes from the bacterium Staphylococcus aureus, for which more than ten entire genomes have been sequenced. We compared these multiple genome sequences at a locus for the lpl (lipoprotein-like) cluster (encoding lipoprotein homologs presumably related to their host interaction) in the genomic island termed nuSaalpha. A highly conserved nucleotide sequence found within every lpl ORF is likely to provide a site for homologous recombination. Comparison of phylogenies of the 5'-variable region and the 3'-variable region within the same ORF revealed significant incongruence. In contrast, pairs of the 3'-variable region of an ORF and the 5'-variable region of the next downstream ORF gave more congruent phylogenies, with distinct groups of conserved pairs. The intergenic region seemed to have coevolved with the flanking variable regions. Multiple recombination events at the central conserved region appear to have caused various types of rearrangements among strains, shuffling the two variable regions in one ORF, but maintaining a conserved unit comprising the 3'-variable region, the intergenic region, and the 5'-variable region spanning adjacent ORFs. This result has strong impact on our understanding of gene evolution because most gene lineages underwent tandem duplication and then diversified. This work also illustrates the use of multiple genome sequences for high-resolution evolutionary analysis within the same species.

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Related in: MedlinePlus

Maps of SA1317 homolog clusters in various Staphylococcus aureus strains. The SA1317 homologs are drawn in bold lines. Naming of their 5′-variable region and 3′-variable region is after the tree-based grouping in figure 9. The larger intervening ORF, SAU1320 and its homologous genes, is observed in all the strains except for MRSA252, whereas the shorter intervening ORF, SAA1377 and its homologs, is observed in strains USA300, COL, and NCTC8325. SAB1350 and SAB1349 in RF122 are truncated genes homologous to SAU1320. Insertion of a prophage into the larger intervening ORF observed in USA300, NCTC8325, and MW2 is indicated by a black triangle.
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fig10: Maps of SA1317 homolog clusters in various Staphylococcus aureus strains. The SA1317 homologs are drawn in bold lines. Naming of their 5′-variable region and 3′-variable region is after the tree-based grouping in figure 9. The larger intervening ORF, SAU1320 and its homologous genes, is observed in all the strains except for MRSA252, whereas the shorter intervening ORF, SAA1377 and its homologs, is observed in strains USA300, COL, and NCTC8325. SAB1350 and SAB1349 in RF122 are truncated genes homologous to SAU1320. Insertion of a prophage into the larger intervening ORF observed in USA300, NCTC8325, and MW2 is indicated by a black triangle.

Mentions: The above definitions related to gene structure and phylogenetic comparison were repeated for another tandem gene cluster for hypothetical proteins, homologs of SA1317 (figs. 8–10). Grouping was carried out for each of the two variable regions separately so as the mutual evolutionary distance remains equal to or shorter than 0.15 within a group (fig. 9).


Multiple genome comparison within a bacterial species reveals a unit of evolution spanning two adjacent genes in a tandem paralog cluster.

Tsuru T, Kobayashi I - Mol. Biol. Evol. (2008)

Maps of SA1317 homolog clusters in various Staphylococcus aureus strains. The SA1317 homologs are drawn in bold lines. Naming of their 5′-variable region and 3′-variable region is after the tree-based grouping in figure 9. The larger intervening ORF, SAU1320 and its homologous genes, is observed in all the strains except for MRSA252, whereas the shorter intervening ORF, SAA1377 and its homologs, is observed in strains USA300, COL, and NCTC8325. SAB1350 and SAB1349 in RF122 are truncated genes homologous to SAU1320. Insertion of a prophage into the larger intervening ORF observed in USA300, NCTC8325, and MW2 is indicated by a black triangle.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2568036&req=5

fig10: Maps of SA1317 homolog clusters in various Staphylococcus aureus strains. The SA1317 homologs are drawn in bold lines. Naming of their 5′-variable region and 3′-variable region is after the tree-based grouping in figure 9. The larger intervening ORF, SAU1320 and its homologous genes, is observed in all the strains except for MRSA252, whereas the shorter intervening ORF, SAA1377 and its homologs, is observed in strains USA300, COL, and NCTC8325. SAB1350 and SAB1349 in RF122 are truncated genes homologous to SAU1320. Insertion of a prophage into the larger intervening ORF observed in USA300, NCTC8325, and MW2 is indicated by a black triangle.
Mentions: The above definitions related to gene structure and phylogenetic comparison were repeated for another tandem gene cluster for hypothetical proteins, homologs of SA1317 (figs. 8–10). Grouping was carried out for each of the two variable regions separately so as the mutual evolutionary distance remains equal to or shorter than 0.15 within a group (fig. 9).

Bottom Line: A highly conserved nucleotide sequence found within every lpl ORF is likely to provide a site for homologous recombination.This result has strong impact on our understanding of gene evolution because most gene lineages underwent tandem duplication and then diversified.This work also illustrates the use of multiple genome sequences for high-resolution evolutionary analysis within the same species.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Social Genome Sciences, Department of Medical Genome Sciences, Graduate School of Frontier Sciences, University of Tokyo, Tokyo, Japan.

ABSTRACT
It has been assumed that an open reading frame (ORF) represents a unit of gene evolution as well as a unit of gene expression and function. In the present work, we report a case in which a unit comprising the 3' region of an ORF linked to a downstream intergenic region that is in turn linked to the 5' region of a downstream ORF has been conserved, and has served as the unit of gene evolution. The genes are tandem paralogous genes from the bacterium Staphylococcus aureus, for which more than ten entire genomes have been sequenced. We compared these multiple genome sequences at a locus for the lpl (lipoprotein-like) cluster (encoding lipoprotein homologs presumably related to their host interaction) in the genomic island termed nuSaalpha. A highly conserved nucleotide sequence found within every lpl ORF is likely to provide a site for homologous recombination. Comparison of phylogenies of the 5'-variable region and the 3'-variable region within the same ORF revealed significant incongruence. In contrast, pairs of the 3'-variable region of an ORF and the 5'-variable region of the next downstream ORF gave more congruent phylogenies, with distinct groups of conserved pairs. The intergenic region seemed to have coevolved with the flanking variable regions. Multiple recombination events at the central conserved region appear to have caused various types of rearrangements among strains, shuffling the two variable regions in one ORF, but maintaining a conserved unit comprising the 3'-variable region, the intergenic region, and the 5'-variable region spanning adjacent ORFs. This result has strong impact on our understanding of gene evolution because most gene lineages underwent tandem duplication and then diversified. This work also illustrates the use of multiple genome sequences for high-resolution evolutionary analysis within the same species.

Show MeSH
Related in: MedlinePlus