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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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Allocation of B. cenocepacia strain J2315 σ 70 deduced factors into the main σ 70 gene family phylogenetic groups. All Bcen-J2315 deduced amino acids sequences from σ70 coding sequences were added to the frame of the Lavire et al. [13] multiple alignment. A Neighbor-joining phylogenetic tree was computed from this multiple alignment. Distances on this tree are proportional to evolutionary divergences expressed in substitutions per 100 sites. The Bcen-J2315 sequences were allocated to one of the following phylogenetic groups: group 1, the essential primary factors, and alternative primary factors of the actinobacteria; group 2, stationary phase factors of the RpoS type; group 3, factors involved in heat shock response, flagella synthesis or cellular differentiation, and group 4, factors involved in extracytoplasmic functions (ECF).
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Figure 1: Allocation of B. cenocepacia strain J2315 σ 70 deduced factors into the main σ 70 gene family phylogenetic groups. All Bcen-J2315 deduced amino acids sequences from σ70 coding sequences were added to the frame of the Lavire et al. [13] multiple alignment. A Neighbor-joining phylogenetic tree was computed from this multiple alignment. Distances on this tree are proportional to evolutionary divergences expressed in substitutions per 100 sites. The Bcen-J2315 sequences were allocated to one of the following phylogenetic groups: group 1, the essential primary factors, and alternative primary factors of the actinobacteria; group 2, stationary phase factors of the RpoS type; group 3, factors involved in heat shock response, flagella synthesis or cellular differentiation, and group 4, factors involved in extracytoplasmic functions (ECF).

Mentions: Translated amino acid (AA) sequences from Bcen-J2315 σ70 coding sequences were positioned among the main eubacterial σ70 lineages, using a decisional σ70 Neighbor-Joining (NJ) phylogenetic tree limited to key sequences (Fig. 1). This phylogenetic tree divides the σ70 gene family into four groups (see [13]): (1) one grouping the primary (mainly RpoD) and alternative primary actinomycetal factors, (2) one grouping the stationary phase factors (mainly named RpoS), (3) one the heat shock (RpoH), flagellin (FliA), and cellular differentiation (WhiG) factors, and (4) one grouping factors involved in extracytoplasmic functions (named ECF factors). All these groups are supported by high bootstrap values. This phylogenetic tree allowed to allocate 14 of the Bcen-J2315 σ70 gene sequences into the ECF (see Table 1). The ECF group is often the most important in number, and is the main group involved in bacterial responses toward changing environmental conditions. ECF sequences represent 66% of the σ70 gene sequences of the Bcen-J2315 genome, a number which is lower than the one observed in P. aeruginosa (82%) [6,15]. Two deduced AA sequences, EcfA1 and EcfA2, are 100% identical in Bcen-J2315, and their respective genes are positioned on two identical DNA strands of 40 kb that are diametrically opposed on chromosome 1 (see section on ecfA for further details). For the remaining 6 factors, three were allocated to group 1 (SigE, SigI and SigJ), one to group 2 (SigK), and two to group 3 (SigL and SigM).


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)

Allocation of B. cenocepacia strain J2315 σ 70 deduced factors into the main σ 70 gene family phylogenetic groups. All Bcen-J2315 deduced amino acids sequences from σ70 coding sequences were added to the frame of the Lavire et al. [13] multiple alignment. A Neighbor-joining phylogenetic tree was computed from this multiple alignment. Distances on this tree are proportional to evolutionary divergences expressed in substitutions per 100 sites. The Bcen-J2315 sequences were allocated to one of the following phylogenetic groups: group 1, the essential primary factors, and alternative primary factors of the actinobacteria; group 2, stationary phase factors of the RpoS type; group 3, factors involved in heat shock response, flagella synthesis or cellular differentiation, and group 4, factors involved in extracytoplasmic functions (ECF).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Allocation of B. cenocepacia strain J2315 σ 70 deduced factors into the main σ 70 gene family phylogenetic groups. All Bcen-J2315 deduced amino acids sequences from σ70 coding sequences were added to the frame of the Lavire et al. [13] multiple alignment. A Neighbor-joining phylogenetic tree was computed from this multiple alignment. Distances on this tree are proportional to evolutionary divergences expressed in substitutions per 100 sites. The Bcen-J2315 sequences were allocated to one of the following phylogenetic groups: group 1, the essential primary factors, and alternative primary factors of the actinobacteria; group 2, stationary phase factors of the RpoS type; group 3, factors involved in heat shock response, flagella synthesis or cellular differentiation, and group 4, factors involved in extracytoplasmic functions (ECF).
Mentions: Translated amino acid (AA) sequences from Bcen-J2315 σ70 coding sequences were positioned among the main eubacterial σ70 lineages, using a decisional σ70 Neighbor-Joining (NJ) phylogenetic tree limited to key sequences (Fig. 1). This phylogenetic tree divides the σ70 gene family into four groups (see [13]): (1) one grouping the primary (mainly RpoD) and alternative primary actinomycetal factors, (2) one grouping the stationary phase factors (mainly named RpoS), (3) one the heat shock (RpoH), flagellin (FliA), and cellular differentiation (WhiG) factors, and (4) one grouping factors involved in extracytoplasmic functions (named ECF factors). All these groups are supported by high bootstrap values. This phylogenetic tree allowed to allocate 14 of the Bcen-J2315 σ70 gene sequences into the ECF (see Table 1). The ECF group is often the most important in number, and is the main group involved in bacterial responses toward changing environmental conditions. ECF sequences represent 66% of the σ70 gene sequences of the Bcen-J2315 genome, a number which is lower than the one observed in P. aeruginosa (82%) [6,15]. Two deduced AA sequences, EcfA1 and EcfA2, are 100% identical in Bcen-J2315, and their respective genes are positioned on two identical DNA strands of 40 kb that are diametrically opposed on chromosome 1 (see section on ecfA for further details). For the remaining 6 factors, three were allocated to group 1 (SigE, SigI and SigJ), one to group 2 (SigK), and two to group 3 (SigL and SigM).

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