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Architecture of Burkholderia cepacia complex sigma70 gene family: evidence of alternative primary and clade-specific factors, and genomic instability.

Menard A, de Los Santos PE, Graindorge A, Cournoyer B - BMC Genomics (2007)

Bottom Line: This number is lower than the one of Pseudomonas aeruginosa, a species found in similar habitats including CF lungs.The Bcc sigma70 gene family was found to be under strong selective pressures that could lead to acquisition/deletion, and duplication events modifying its architecture.Comparative analysis of Bcc and Pseudomonas aeruginosa sigma70 gene families revealed distinct evolutionary strategies, with the Bcc having selected several alternative primary factors, something not recorded among P. aeruginosa and only previously reported to occur among the actinobacteria.

View Article: PubMed Central - HTML - PubMed

Affiliation: Université de Lyon, Lyon, France. menard@biomserv.univ-lyon1.fr

ABSTRACT

Background: The Burkholderia cepacia complex (Bcc) groups bacterial species with beneficial properties that can improve crop yields or remediate polluted sites but can also lead to dramatic human clinical outcomes among cystic fibrosis (CF) or immuno-compromised individuals. Genome-wide regulatory processes of gene expression could explain parts of this bacterial duality. Transcriptional sigma70 factors are components of these processes. They allow the reversible binding of the DNA-dependent RNA polymerase to form the holoenzyme that will lead to mRNA synthesis from a DNA promoter region. Bcc genome-wide analyses were performed to investigate the major evolutionary trends taking place in the sigma70 family of these bacteria.

Results: Twenty sigma70 paralogous genes were detected in the Burkholderia cenocepacia strain J2315 (Bcen-J2315) genome, of which 14 were of the ECF (extracytoplasmic function) group. Non-ECF paralogs were related to primary (rpoD), alternative primary, stationary phase (rpoS), flagellin biosynthesis (fliA), and heat shock (rpoH) factors. The number of sigma70 genetic determinants among this genome was of 2,86 per Mb. This number is lower than the one of Pseudomonas aeruginosa, a species found in similar habitats including CF lungs. These two bacterial groups showed strikingly different sigma70 family architectures, with only three ECF paralogs in common (fecI-like, pvdS and algU). Bcen-J2315 sigma70 paralogs showed clade-specific distributions. Some paralogs appeared limited to the ET12 epidemic clone (ecfA2), particular Bcc species (sigI), the Burkholderia genus (ecfJ, ecfF, and sigJ), certain proteobacterial groups (ecfA1, ecfC, ecfD, ecfE, ecfG, ecfL, ecfM and rpoS), or were broadly distributed in the eubacteria (ecfI, ecfK, ecfH, ecfB, and rpoD-, rpoH-, fliA-like genes). Genomic instability of this gene family was driven by chromosomal inversion (ecfA2), recent duplication events (ecfA and RpoD), localized (ecfG) and large scale deletions (sigI, sigJ, ecfC, ecfH, and ecfK), and a phage integration event (ecfE).

Conclusion: The Bcc sigma70 gene family was found to be under strong selective pressures that could lead to acquisition/deletion, and duplication events modifying its architecture. Comparative analysis of Bcc and Pseudomonas aeruginosa sigma70 gene families revealed distinct evolutionary strategies, with the Bcc having selected several alternative primary factors, something not recorded among P. aeruginosa and only previously reported to occur among the actinobacteria.

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Neighbor-Joining phylogenic tree of ECF σ 70 factors. The sequences were retrieved from sequenced Burkholderia genomes or the GenBank database. Within one species, when sequences were orthologs, only one sequence per sigma factor was kept. A total of 746 sites were analyzed (with pairwise deletion of gap-containing sites). Distances are proportional to evolutionary divergences expressed in substitutions per 100 sites. Bootstrap values higher than 85% are given. Distribution among other proteobacterial groups is indicated. Likely role of the identified ECF factors is indicated.
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Figure 4: Neighbor-Joining phylogenic tree of ECF σ 70 factors. The sequences were retrieved from sequenced Burkholderia genomes or the GenBank database. Within one species, when sequences were orthologs, only one sequence per sigma factor was kept. A total of 746 sites were analyzed (with pairwise deletion of gap-containing sites). Distances are proportional to evolutionary divergences expressed in substitutions per 100 sites. Bootstrap values higher than 85% are given. Distribution among other proteobacterial groups is indicated. Likely role of the identified ECF factors is indicated.

Mentions: Phylogenetic relationships among the ECF cluster are presented in Fig. 4. All database sequences closely related to Bcen-J2315 putative ECF were considered in this analysis. A first round of phylogenetic analysis allowed the identification of all database factors related to Bcen-J2315 ECFs. A second round of analyses was then performed by limiting the dataset to a set of selected sequences representative of the main phylogenetic trends observed. Fig. 4 shows the best NJ tree obtained. Its structure is not supported by high bootstrap values but all sub-groups of ECFs are supported by high ones. EcfA, EcfC and EcfI deduced AA sequences are the only Bcen-J2315 ECF factors having homologs in the P. aeruginosa genomes.


Architecture of Burkholderia cepacia complex sigma70 gene family: evidence of alternative primary and clade-specific factors, and genomic instability.

Menard A, de Los Santos PE, Graindorge A, Cournoyer B - BMC Genomics (2007)

Neighbor-Joining phylogenic tree of ECF σ 70 factors. The sequences were retrieved from sequenced Burkholderia genomes or the GenBank database. Within one species, when sequences were orthologs, only one sequence per sigma factor was kept. A total of 746 sites were analyzed (with pairwise deletion of gap-containing sites). Distances are proportional to evolutionary divergences expressed in substitutions per 100 sites. Bootstrap values higher than 85% are given. Distribution among other proteobacterial groups is indicated. Likely role of the identified ECF factors is indicated.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2194791&req=5

Figure 4: Neighbor-Joining phylogenic tree of ECF σ 70 factors. The sequences were retrieved from sequenced Burkholderia genomes or the GenBank database. Within one species, when sequences were orthologs, only one sequence per sigma factor was kept. A total of 746 sites were analyzed (with pairwise deletion of gap-containing sites). Distances are proportional to evolutionary divergences expressed in substitutions per 100 sites. Bootstrap values higher than 85% are given. Distribution among other proteobacterial groups is indicated. Likely role of the identified ECF factors is indicated.
Mentions: Phylogenetic relationships among the ECF cluster are presented in Fig. 4. All database sequences closely related to Bcen-J2315 putative ECF were considered in this analysis. A first round of phylogenetic analysis allowed the identification of all database factors related to Bcen-J2315 ECFs. A second round of analyses was then performed by limiting the dataset to a set of selected sequences representative of the main phylogenetic trends observed. Fig. 4 shows the best NJ tree obtained. Its structure is not supported by high bootstrap values but all sub-groups of ECFs are supported by high ones. EcfA, EcfC and EcfI deduced AA sequences are the only Bcen-J2315 ECF factors having homologs in the P. aeruginosa genomes.

Bottom Line: This number is lower than the one of Pseudomonas aeruginosa, a species found in similar habitats including CF lungs.The Bcc sigma70 gene family was found to be under strong selective pressures that could lead to acquisition/deletion, and duplication events modifying its architecture.Comparative analysis of Bcc and Pseudomonas aeruginosa sigma70 gene families revealed distinct evolutionary strategies, with the Bcc having selected several alternative primary factors, something not recorded among P. aeruginosa and only previously reported to occur among the actinobacteria.

View Article: PubMed Central - HTML - PubMed

Affiliation: Université de Lyon, Lyon, France. menard@biomserv.univ-lyon1.fr

ABSTRACT

Background: The Burkholderia cepacia complex (Bcc) groups bacterial species with beneficial properties that can improve crop yields or remediate polluted sites but can also lead to dramatic human clinical outcomes among cystic fibrosis (CF) or immuno-compromised individuals. Genome-wide regulatory processes of gene expression could explain parts of this bacterial duality. Transcriptional sigma70 factors are components of these processes. They allow the reversible binding of the DNA-dependent RNA polymerase to form the holoenzyme that will lead to mRNA synthesis from a DNA promoter region. Bcc genome-wide analyses were performed to investigate the major evolutionary trends taking place in the sigma70 family of these bacteria.

Results: Twenty sigma70 paralogous genes were detected in the Burkholderia cenocepacia strain J2315 (Bcen-J2315) genome, of which 14 were of the ECF (extracytoplasmic function) group. Non-ECF paralogs were related to primary (rpoD), alternative primary, stationary phase (rpoS), flagellin biosynthesis (fliA), and heat shock (rpoH) factors. The number of sigma70 genetic determinants among this genome was of 2,86 per Mb. This number is lower than the one of Pseudomonas aeruginosa, a species found in similar habitats including CF lungs. These two bacterial groups showed strikingly different sigma70 family architectures, with only three ECF paralogs in common (fecI-like, pvdS and algU). Bcen-J2315 sigma70 paralogs showed clade-specific distributions. Some paralogs appeared limited to the ET12 epidemic clone (ecfA2), particular Bcc species (sigI), the Burkholderia genus (ecfJ, ecfF, and sigJ), certain proteobacterial groups (ecfA1, ecfC, ecfD, ecfE, ecfG, ecfL, ecfM and rpoS), or were broadly distributed in the eubacteria (ecfI, ecfK, ecfH, ecfB, and rpoD-, rpoH-, fliA-like genes). Genomic instability of this gene family was driven by chromosomal inversion (ecfA2), recent duplication events (ecfA and RpoD), localized (ecfG) and large scale deletions (sigI, sigJ, ecfC, ecfH, and ecfK), and a phage integration event (ecfE).

Conclusion: The Bcc sigma70 gene family was found to be under strong selective pressures that could lead to acquisition/deletion, and duplication events modifying its architecture. Comparative analysis of Bcc and Pseudomonas aeruginosa sigma70 gene families revealed distinct evolutionary strategies, with the Bcc having selected several alternative primary factors, something not recorded among P. aeruginosa and only previously reported to occur among the actinobacteria.

Show MeSH
Related in: MedlinePlus