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Assessing the evolutionary rate of positional orthologous genes in prokaryotes using synteny data.

Lemoine F, Lespinet O, Labedan B - BMC Evol. Biol. (2007)

Bottom Line: Once all these synteny blocks have been detected, we showed that POGs are subject to more evolutionary constraints than orthologs outside synteny groups, whichever the taxonomic distance separating the compared organisms.The suite of programs described in this paper allows a reliable detection of orthologs and is useful for evaluating gene order conservation in prokaryotes whichever their taxonomic distance.Thus, our approach will make easy the rapid identification of POGS in the next few years as we are expecting to be inundated with thousands of completely sequenced microbial genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institut de Génétique et Microbiologie, CNRS UMR 8621, Bâtiment 400, Université Paris Sud XI, 91405 Orsay Cedex, France. frederic.lemoine@igmors.u-psud.fr

ABSTRACT

Background: Comparison of completely sequenced microbial genomes has revealed how fluid these genomes are. Detecting synteny blocks requires reliable methods to determining the orthologs among the whole set of homologs detected by exhaustive comparisons between each pair of completely sequenced genomes. This is a complex and difficult problem in the field of comparative genomics but will help to better understand the way prokaryotic genomes are evolving.

Results: We have developed a suite of programs that automate three essential steps to study conservation of gene order, and validated them with a set of 107 bacteria and archaea that cover the majority of the prokaryotic taxonomic space. We identified the whole set of shared homologs between two or more species and computed the evolutionary distance separating each pair of homologs. We applied two strategies to extract from the set of homologs a collection of valid orthologs shared by at least two genomes. The first computes the Reciprocal Smallest Distance (RSD) using the PAM distances separating pairs of homologs. The second method groups homologs in families and reconstructs each family's evolutionary tree, distinguishing bona fide orthologs as well as paralogs created after the last speciation event. Although the phylogenetic tree method often succeeds where RSD fails, the reverse could occasionally be true. Accordingly, we used the data obtained with either methods or their intersection to number the orthologs that are adjacent in for each pair of genomes, the Positional Orthologous Genes (POGs), and to further study their properties. Once all these synteny blocks have been detected, we showed that POGs are subject to more evolutionary constraints than orthologs outside synteny groups, whichever the taxonomic distance separating the compared organisms.

Conclusion: The suite of programs described in this paper allows a reliable detection of orthologs and is useful for evaluating gene order conservation in prokaryotes whichever their taxonomic distance. Thus, our approach will make easy the rapid identification of POGS in the next few years as we are expecting to be inundated with thousands of completely sequenced microbial genomes.

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Comparing the distribution of PAM distances separating pairs of orthologs shared between the proteomes of E. coli and four other organisms. Panel A (upper part) shows the respective distributions of the PAM distances for all pairs of orthologs shared by E. coli and S. enterica, B. subtilis, B. thetaiotaomicron and M. acetivorans, respectively. The color code is given in box B, which also compares the respective mean of each PAM distance distribution and the total number of orthologs shared by each pair of genomes analyzed in A.
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Figure 3: Comparing the distribution of PAM distances separating pairs of orthologs shared between the proteomes of E. coli and four other organisms. Panel A (upper part) shows the respective distributions of the PAM distances for all pairs of orthologs shared by E. coli and S. enterica, B. subtilis, B. thetaiotaomicron and M. acetivorans, respectively. The color code is given in box B, which also compares the respective mean of each PAM distance distribution and the total number of orthologs shared by each pair of genomes analyzed in A.

Mentions: The PAM distance that separates two orthologs in various pairs of genomes was used to compare the rate of evolution of different classes of orthologs with different respects. First, Fig. 3A shows the distribution of the PAM distances separating orthologous pairs when comparing E. coli with closely related Enterobacteriaceae S. enterica, the Firmicute B. subtilis, the member of the Bacteroidetes/Chlorobi group Bacteroides thetaiotaomicron and the archaeon M. acetivorans. As expected, this distribution is very dependent of the taxonomic proximity between species. This is confirmed in Fig. 3B and Table 3 that display the taxonomic distributions of the mean of the PAM distances separating pairs of orthologs and of the total number of orthologous pairs in the different genomic comparisons.


Assessing the evolutionary rate of positional orthologous genes in prokaryotes using synteny data.

Lemoine F, Lespinet O, Labedan B - BMC Evol. Biol. (2007)

Comparing the distribution of PAM distances separating pairs of orthologs shared between the proteomes of E. coli and four other organisms. Panel A (upper part) shows the respective distributions of the PAM distances for all pairs of orthologs shared by E. coli and S. enterica, B. subtilis, B. thetaiotaomicron and M. acetivorans, respectively. The color code is given in box B, which also compares the respective mean of each PAM distance distribution and the total number of orthologs shared by each pair of genomes analyzed in A.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2238764&req=5

Figure 3: Comparing the distribution of PAM distances separating pairs of orthologs shared between the proteomes of E. coli and four other organisms. Panel A (upper part) shows the respective distributions of the PAM distances for all pairs of orthologs shared by E. coli and S. enterica, B. subtilis, B. thetaiotaomicron and M. acetivorans, respectively. The color code is given in box B, which also compares the respective mean of each PAM distance distribution and the total number of orthologs shared by each pair of genomes analyzed in A.
Mentions: The PAM distance that separates two orthologs in various pairs of genomes was used to compare the rate of evolution of different classes of orthologs with different respects. First, Fig. 3A shows the distribution of the PAM distances separating orthologous pairs when comparing E. coli with closely related Enterobacteriaceae S. enterica, the Firmicute B. subtilis, the member of the Bacteroidetes/Chlorobi group Bacteroides thetaiotaomicron and the archaeon M. acetivorans. As expected, this distribution is very dependent of the taxonomic proximity between species. This is confirmed in Fig. 3B and Table 3 that display the taxonomic distributions of the mean of the PAM distances separating pairs of orthologs and of the total number of orthologous pairs in the different genomic comparisons.

Bottom Line: Once all these synteny blocks have been detected, we showed that POGs are subject to more evolutionary constraints than orthologs outside synteny groups, whichever the taxonomic distance separating the compared organisms.The suite of programs described in this paper allows a reliable detection of orthologs and is useful for evaluating gene order conservation in prokaryotes whichever their taxonomic distance.Thus, our approach will make easy the rapid identification of POGS in the next few years as we are expecting to be inundated with thousands of completely sequenced microbial genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institut de Génétique et Microbiologie, CNRS UMR 8621, Bâtiment 400, Université Paris Sud XI, 91405 Orsay Cedex, France. frederic.lemoine@igmors.u-psud.fr

ABSTRACT

Background: Comparison of completely sequenced microbial genomes has revealed how fluid these genomes are. Detecting synteny blocks requires reliable methods to determining the orthologs among the whole set of homologs detected by exhaustive comparisons between each pair of completely sequenced genomes. This is a complex and difficult problem in the field of comparative genomics but will help to better understand the way prokaryotic genomes are evolving.

Results: We have developed a suite of programs that automate three essential steps to study conservation of gene order, and validated them with a set of 107 bacteria and archaea that cover the majority of the prokaryotic taxonomic space. We identified the whole set of shared homologs between two or more species and computed the evolutionary distance separating each pair of homologs. We applied two strategies to extract from the set of homologs a collection of valid orthologs shared by at least two genomes. The first computes the Reciprocal Smallest Distance (RSD) using the PAM distances separating pairs of homologs. The second method groups homologs in families and reconstructs each family's evolutionary tree, distinguishing bona fide orthologs as well as paralogs created after the last speciation event. Although the phylogenetic tree method often succeeds where RSD fails, the reverse could occasionally be true. Accordingly, we used the data obtained with either methods or their intersection to number the orthologs that are adjacent in for each pair of genomes, the Positional Orthologous Genes (POGs), and to further study their properties. Once all these synteny blocks have been detected, we showed that POGs are subject to more evolutionary constraints than orthologs outside synteny groups, whichever the taxonomic distance separating the compared organisms.

Conclusion: The suite of programs described in this paper allows a reliable detection of orthologs and is useful for evaluating gene order conservation in prokaryotes whichever their taxonomic distance. Thus, our approach will make easy the rapid identification of POGS in the next few years as we are expecting to be inundated with thousands of completely sequenced microbial genomes.

Show MeSH