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IS4 family goes genomic.

De Palmenaer D, Siguier P, Mahillon J - BMC Evol. Biol. (2008)

Bottom Line: Significant expansions were detected only in some pathogens as well as among certain extremophiles, suggesting the probable involvement of some elements in bacterial and archaeal adaptation and/or evolution.The present taxonomic update of IS4 and emerging families will facilitate the classification of future elements as they arise from ongoing genome sequencing.Their narrow genomic impact and the existence of both IS-poor and IS-rich thriving prokaryotes suggested that these families, and probably ISs in general, are occasionally used as a tool for genome flexibility and evolution, rather than just representing self sustaining DNA entities.

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Affiliation: Laboratoire de microbiologie alimentaire et environnementale, Université catholique de Louvain, Croix du Sud 2/12, B-1348 Louvain-la-Neuve, Belgium. daniel.depalmenaer@uclouvain.be

ABSTRACT

Background: Insertion sequences (ISs) are small, mobile DNA entities able to expand in prokaryotic genomes and trigger important rearrangements. To understand their role in evolution, accurate IS taxonomy is essential. The IS4 family is composed of approximately 70 elements and, like some other families, displays extremely elevated levels of internal divergence impeding its classification. The increasing availability of complete genome sequences provides a valuable source for the discovery of additional IS4 elements. In this study, this genomic database was used to update the structural and functional definition of the IS4 family.

Results: A total of 227 IS4-related sequences were collected among more than 500 sequenced bacterial and archaeal genomes, representing more than a three fold increase of the initial inventory. A clear division into seven coherent subgroups was discovered as well as three emerging families, which displayed distinct structural and functional properties. The IS4 family was sporadically present in 17 % of analyzed genomes, with most of them displaying single or a small number of IS4 elements. Significant expansions were detected only in some pathogens as well as among certain extremophiles, suggesting the probable involvement of some elements in bacterial and archaeal adaptation and/or evolution. Finally, it should be noted that some IS4 subgroups and two emerging families occurred preferentially in specific phyla or exclusively inside a specific genus.

Conclusion: The present taxonomic update of IS4 and emerging families will facilitate the classification of future elements as they arise from ongoing genome sequencing. Their narrow genomic impact and the existence of both IS-poor and IS-rich thriving prokaryotes suggested that these families, and probably ISs in general, are occasionally used as a tool for genome flexibility and evolution, rather than just representing self sustaining DNA entities.

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Prokaryote distribution of IS4 subgroups and emerging families. A. Three dimensional histogram of the number of distinct elements belonging to IS4 subgroups and emerging families, as they can be found among major prokaryotic clades. Each IS subgroup/family is represented by a different color. Iso-forms (which we defined as elements that show a divergence of less than 2% in the amino acid sequence of their potential proteins) were not included. The line 'Others' stands for Aquificae, Chlamydiae/Verrucomicrobia, Chloroflexi, Chrysiogenetes, Dictyoglomi, Fusobacteria, Nitrospirae, Spirochetes, Thermodesulfobacteria and Thermotogae. For interpretation, see main text. B. To avoid misinterpretation triggered by unequal sequencing efforts between different microbial groups, the number of genome projects, as of 1st April 2007, is depicted by histogram.
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Figure 4: Prokaryote distribution of IS4 subgroups and emerging families. A. Three dimensional histogram of the number of distinct elements belonging to IS4 subgroups and emerging families, as they can be found among major prokaryotic clades. Each IS subgroup/family is represented by a different color. Iso-forms (which we defined as elements that show a divergence of less than 2% in the amino acid sequence of their potential proteins) were not included. The line 'Others' stands for Aquificae, Chlamydiae/Verrucomicrobia, Chloroflexi, Chrysiogenetes, Dictyoglomi, Fusobacteria, Nitrospirae, Spirochetes, Thermodesulfobacteria and Thermotogae. For interpretation, see main text. B. To avoid misinterpretation triggered by unequal sequencing efforts between different microbial groups, the number of genome projects, as of 1st April 2007, is depicted by histogram.

Mentions: Subgroup IS231 was previously established (reviewed in reference [2]) and was the most coherent one since many transposase pairs displayed sequence identity percentages above 50 (see also Figure 1A). Likewise, their DNA ends are among the most conserved. A clear relationship was observed between transposase and extremity conservation (Additional file 1). This is particularly true for left extremities (conventionally upstream of the transposase gene) where transposase-related conservation extended beyond the TIRs. The IS231 subgroup further distinguished itself by the fact that its members occurred almost exclusively in genomes of phylogenetically close bacteria composing the B. cereus sensu lato group (i.e. B. cereus sensu stricto, B. thuringiensis and B. anthracis, see Additional file 1 and Figure 4). As previously shown, an important hallmark is the large size range of its elements (Table 1). A significant fraction of them displayed additional DNA between the left TIR and the transposase gene [2,3], which is still unusual among ISs. In this study, novel putative passenger genes were found in these extra sequences coding for resistance, virulence or metabolism determinants as well as unknown orfs (results not shown). This modular aspect has not yet been observed in other IS families or IS4 subgroups, which may be due to the fact that, so far, no systematic and thorough searches for supplementary IS DNA were carried out in other families.


IS4 family goes genomic.

De Palmenaer D, Siguier P, Mahillon J - BMC Evol. Biol. (2008)

Prokaryote distribution of IS4 subgroups and emerging families. A. Three dimensional histogram of the number of distinct elements belonging to IS4 subgroups and emerging families, as they can be found among major prokaryotic clades. Each IS subgroup/family is represented by a different color. Iso-forms (which we defined as elements that show a divergence of less than 2% in the amino acid sequence of their potential proteins) were not included. The line 'Others' stands for Aquificae, Chlamydiae/Verrucomicrobia, Chloroflexi, Chrysiogenetes, Dictyoglomi, Fusobacteria, Nitrospirae, Spirochetes, Thermodesulfobacteria and Thermotogae. For interpretation, see main text. B. To avoid misinterpretation triggered by unequal sequencing efforts between different microbial groups, the number of genome projects, as of 1st April 2007, is depicted by histogram.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2266710&req=5

Figure 4: Prokaryote distribution of IS4 subgroups and emerging families. A. Three dimensional histogram of the number of distinct elements belonging to IS4 subgroups and emerging families, as they can be found among major prokaryotic clades. Each IS subgroup/family is represented by a different color. Iso-forms (which we defined as elements that show a divergence of less than 2% in the amino acid sequence of their potential proteins) were not included. The line 'Others' stands for Aquificae, Chlamydiae/Verrucomicrobia, Chloroflexi, Chrysiogenetes, Dictyoglomi, Fusobacteria, Nitrospirae, Spirochetes, Thermodesulfobacteria and Thermotogae. For interpretation, see main text. B. To avoid misinterpretation triggered by unequal sequencing efforts between different microbial groups, the number of genome projects, as of 1st April 2007, is depicted by histogram.
Mentions: Subgroup IS231 was previously established (reviewed in reference [2]) and was the most coherent one since many transposase pairs displayed sequence identity percentages above 50 (see also Figure 1A). Likewise, their DNA ends are among the most conserved. A clear relationship was observed between transposase and extremity conservation (Additional file 1). This is particularly true for left extremities (conventionally upstream of the transposase gene) where transposase-related conservation extended beyond the TIRs. The IS231 subgroup further distinguished itself by the fact that its members occurred almost exclusively in genomes of phylogenetically close bacteria composing the B. cereus sensu lato group (i.e. B. cereus sensu stricto, B. thuringiensis and B. anthracis, see Additional file 1 and Figure 4). As previously shown, an important hallmark is the large size range of its elements (Table 1). A significant fraction of them displayed additional DNA between the left TIR and the transposase gene [2,3], which is still unusual among ISs. In this study, novel putative passenger genes were found in these extra sequences coding for resistance, virulence or metabolism determinants as well as unknown orfs (results not shown). This modular aspect has not yet been observed in other IS families or IS4 subgroups, which may be due to the fact that, so far, no systematic and thorough searches for supplementary IS DNA were carried out in other families.

Bottom Line: Significant expansions were detected only in some pathogens as well as among certain extremophiles, suggesting the probable involvement of some elements in bacterial and archaeal adaptation and/or evolution.The present taxonomic update of IS4 and emerging families will facilitate the classification of future elements as they arise from ongoing genome sequencing.Their narrow genomic impact and the existence of both IS-poor and IS-rich thriving prokaryotes suggested that these families, and probably ISs in general, are occasionally used as a tool for genome flexibility and evolution, rather than just representing self sustaining DNA entities.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratoire de microbiologie alimentaire et environnementale, Université catholique de Louvain, Croix du Sud 2/12, B-1348 Louvain-la-Neuve, Belgium. daniel.depalmenaer@uclouvain.be

ABSTRACT

Background: Insertion sequences (ISs) are small, mobile DNA entities able to expand in prokaryotic genomes and trigger important rearrangements. To understand their role in evolution, accurate IS taxonomy is essential. The IS4 family is composed of approximately 70 elements and, like some other families, displays extremely elevated levels of internal divergence impeding its classification. The increasing availability of complete genome sequences provides a valuable source for the discovery of additional IS4 elements. In this study, this genomic database was used to update the structural and functional definition of the IS4 family.

Results: A total of 227 IS4-related sequences were collected among more than 500 sequenced bacterial and archaeal genomes, representing more than a three fold increase of the initial inventory. A clear division into seven coherent subgroups was discovered as well as three emerging families, which displayed distinct structural and functional properties. The IS4 family was sporadically present in 17 % of analyzed genomes, with most of them displaying single or a small number of IS4 elements. Significant expansions were detected only in some pathogens as well as among certain extremophiles, suggesting the probable involvement of some elements in bacterial and archaeal adaptation and/or evolution. Finally, it should be noted that some IS4 subgroups and two emerging families occurred preferentially in specific phyla or exclusively inside a specific genus.

Conclusion: The present taxonomic update of IS4 and emerging families will facilitate the classification of future elements as they arise from ongoing genome sequencing. Their narrow genomic impact and the existence of both IS-poor and IS-rich thriving prokaryotes suggested that these families, and probably ISs in general, are occasionally used as a tool for genome flexibility and evolution, rather than just representing self sustaining DNA entities.

Show MeSH
Related in: MedlinePlus