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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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Structure of lpl genes (top) with similarity plots for nucleotide sequences (middle) and for amino acid sequences (bottom). The central conserved region is highlighted by gray shading. A predicted signal peptide region is indicated together with a conserved cysteine residue at the C-terminus.
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fig2: Structure of lpl genes (top) with similarity plots for nucleotide sequences (middle) and for amino acid sequences (bottom). The central conserved region is highlighted by gray shading. A predicted signal peptide region is indicated together with a conserved cysteine residue at the C-terminus.

Mentions: The presence of the central conserved region was visualized by similarity plots of aligned nucleotide/amino acid sequences constructed using PLOTCON (http://emboss.sourceforge.net/), in which a similarity score, with window size of 5, was calculated with EDNAFULL score file for nucleotide sequences and with EBLOSUM62 for amino acid sequences (fig. 2). A region conserved both at the nucleotide sequence level and at the amino acid sequence level was determined in the alignments by visual inspection and defined as the central conserved region (supplementary fig. S3A and B, Supplementary Material online). Divergent regions to its 5′ side and to its 3′ side were defined as the 5′-variable region and the 3′-variable region, respectively.


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)

Structure of lpl genes (top) with similarity plots for nucleotide sequences (middle) and for amino acid sequences (bottom). The central conserved region is highlighted by gray shading. A predicted signal peptide region is indicated together with a conserved cysteine residue at the C-terminus.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig2: Structure of lpl genes (top) with similarity plots for nucleotide sequences (middle) and for amino acid sequences (bottom). The central conserved region is highlighted by gray shading. A predicted signal peptide region is indicated together with a conserved cysteine residue at the C-terminus.
Mentions: The presence of the central conserved region was visualized by similarity plots of aligned nucleotide/amino acid sequences constructed using PLOTCON (http://emboss.sourceforge.net/), in which a similarity score, with window size of 5, was calculated with EDNAFULL score file for nucleotide sequences and with EBLOSUM62 for amino acid sequences (fig. 2). A region conserved both at the nucleotide sequence level and at the amino acid sequence level was determined in the alignments by visual inspection and defined as the central conserved region (supplementary fig. S3A and B, Supplementary Material online). Divergent regions to its 5′ side and to its 3′ side were defined as the 5′-variable region and the 3′-variable region, respectively.

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