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Glutamine synthetase sequence evolution in the mycobacteria and their use as molecular markers for Actinobacteria speciation.

Hayward D, van Helden PD, Wiid IJ - BMC Evol. Biol. (2009)

Bottom Line: Intriguingly, previous reports have shown that only one copy (glnA1) is essential for growth in M. tuberculosis, while the other copies (glnA2, glnA3 and glnA4) are not.In this report it is shown that the glnA1 and glnA2 encoded glutamine synthetase sequences were inherited from an Actinobacteria ancestor, while the glnA4 and glnA3 encoded GS sequences were sequentially acquired during Actinobacteria speciation.Different selective pressures by the ecological niche that the organisms occupy may influence the sequence evolution of glnA1 and glnA2 and thereby affecting phylogenies based on the protein sequences they encode.

View Article: PubMed Central - HTML - PubMed

Affiliation: DST/NRF Centre for Excellence in Biomedical Tuberculosis Research, US/MRC Centre for Molecular and Cellular Biology, Division of Molecular Biology and Human Genetics, Faculty of Health Sciences - Stellenbosch University, South Africa. dh@sun.ac.za

ABSTRACT

Background: Although the gene encoding for glutamine synthetase (glnA) is essential in several organisms, multiple glnA copies have been identified in bacterial genomes such as those of the phylum Actinobacteria, notably the mycobacterial species. Intriguingly, previous reports have shown that only one copy (glnA1) is essential for growth in M. tuberculosis, while the other copies (glnA2, glnA3 and glnA4) are not.

Results: In this report it is shown that the glnA1 and glnA2 encoded glutamine synthetase sequences were inherited from an Actinobacteria ancestor, while the glnA4 and glnA3 encoded GS sequences were sequentially acquired during Actinobacteria speciation. The glutamine synthetase sequences encoded by glnA4 and glnA3 are undergoing reductive evolution in the mycobacteria, whilst those encoded by glnA1 and glnA2 are more conserved.

Conclusion: Different selective pressures by the ecological niche that the organisms occupy may influence the sequence evolution of glnA1 and glnA2 and thereby affecting phylogenies based on the protein sequences they encode. The findings in this report may impact the use of similar sequences as molecular markers, as well as shed some light on the evolution of glutamine synthetase in the mycobacteria.

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Dendograms of aligned actinobacterial GSIβ (encoded by glnA1) and GSII (encoded by glnA2) sequences constructed using PAUP 4.0 with the GS sequence of Bifidobacterium longum as out-group (*). Percentage bootstrap support values are shown. The ratio of nonsynonymous (Ka) to synonymous mutations (Ks) in the GS sequences of the mycobacteria and C. diphteria were computed using the GS sequences in C. efficiens, and is shown between brackets.
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Figure 5: Dendograms of aligned actinobacterial GSIβ (encoded by glnA1) and GSII (encoded by glnA2) sequences constructed using PAUP 4.0 with the GS sequence of Bifidobacterium longum as out-group (*). Percentage bootstrap support values are shown. The ratio of nonsynonymous (Ka) to synonymous mutations (Ks) in the GS sequences of the mycobacteria and C. diphteria were computed using the GS sequences in C. efficiens, and is shown between brackets.

Mentions: The lower level of GSIβ sequence conservation observed in comparison to the GSII sequence between species (Table 1) was surprising, since GSIβ may be the major GS of M. tuberculosis and other Actinobacteria [14,15,25]. Since this observation suggests that the GSIβ and GSII sequences evolve differently, Actinobacteria phylogenies based on the GSIβ and GSII sequences were compared to phylogenies based on 16S rRNA sequences [19]. Since the glnA3 and glnA4 protein sequences might be undergoing reductive evolution, they were excluded from the phylogeny. Figure 5 shows that the Actinobacteria phylogeny based on the glnA2-encoded GSII sequence reflects the 16S rRNA phylogeny, while shifts are observed in the phylogeny based on the glnA1-encoded GSIβ sequence. In the GSII sequence phylogeny, organisms are clustered according to suborders, such as the Micrococcineae (B. linens, Arthrobacter, L. xyli, and Janibacter), Corynebacterineae (Corynebacteria sp., Mycobacterium sp., Rhodococcus and N. farcinica), Streptomycineae (Streptomyces sp.), Streptosporangineae (T. fusca) and the Frankineae (A. cellulolyticus, Frankia sp). Exceptions were observed in that K. radiotolerans (Frankineae), P. acnes and Nocardiodes sp. (Propionibacterineae) were dispersed amongst the Micrococcineae. However, bootstrap values below 50 were obtained for these branches making a true interpretation of the inter-relatedness of these organisms impossible. In the phylogenetic tree based on the GSIβ sequence, bootstrap values above 50 were obtained at some of the nodes, but the clustering of organisms to defined Actinobacteria suborders were not observed.


Glutamine synthetase sequence evolution in the mycobacteria and their use as molecular markers for Actinobacteria speciation.

Hayward D, van Helden PD, Wiid IJ - BMC Evol. Biol. (2009)

Dendograms of aligned actinobacterial GSIβ (encoded by glnA1) and GSII (encoded by glnA2) sequences constructed using PAUP 4.0 with the GS sequence of Bifidobacterium longum as out-group (*). Percentage bootstrap support values are shown. The ratio of nonsynonymous (Ka) to synonymous mutations (Ks) in the GS sequences of the mycobacteria and C. diphteria were computed using the GS sequences in C. efficiens, and is shown between brackets.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2667176&req=5

Figure 5: Dendograms of aligned actinobacterial GSIβ (encoded by glnA1) and GSII (encoded by glnA2) sequences constructed using PAUP 4.0 with the GS sequence of Bifidobacterium longum as out-group (*). Percentage bootstrap support values are shown. The ratio of nonsynonymous (Ka) to synonymous mutations (Ks) in the GS sequences of the mycobacteria and C. diphteria were computed using the GS sequences in C. efficiens, and is shown between brackets.
Mentions: The lower level of GSIβ sequence conservation observed in comparison to the GSII sequence between species (Table 1) was surprising, since GSIβ may be the major GS of M. tuberculosis and other Actinobacteria [14,15,25]. Since this observation suggests that the GSIβ and GSII sequences evolve differently, Actinobacteria phylogenies based on the GSIβ and GSII sequences were compared to phylogenies based on 16S rRNA sequences [19]. Since the glnA3 and glnA4 protein sequences might be undergoing reductive evolution, they were excluded from the phylogeny. Figure 5 shows that the Actinobacteria phylogeny based on the glnA2-encoded GSII sequence reflects the 16S rRNA phylogeny, while shifts are observed in the phylogeny based on the glnA1-encoded GSIβ sequence. In the GSII sequence phylogeny, organisms are clustered according to suborders, such as the Micrococcineae (B. linens, Arthrobacter, L. xyli, and Janibacter), Corynebacterineae (Corynebacteria sp., Mycobacterium sp., Rhodococcus and N. farcinica), Streptomycineae (Streptomyces sp.), Streptosporangineae (T. fusca) and the Frankineae (A. cellulolyticus, Frankia sp). Exceptions were observed in that K. radiotolerans (Frankineae), P. acnes and Nocardiodes sp. (Propionibacterineae) were dispersed amongst the Micrococcineae. However, bootstrap values below 50 were obtained for these branches making a true interpretation of the inter-relatedness of these organisms impossible. In the phylogenetic tree based on the GSIβ sequence, bootstrap values above 50 were obtained at some of the nodes, but the clustering of organisms to defined Actinobacteria suborders were not observed.

Bottom Line: Intriguingly, previous reports have shown that only one copy (glnA1) is essential for growth in M. tuberculosis, while the other copies (glnA2, glnA3 and glnA4) are not.In this report it is shown that the glnA1 and glnA2 encoded glutamine synthetase sequences were inherited from an Actinobacteria ancestor, while the glnA4 and glnA3 encoded GS sequences were sequentially acquired during Actinobacteria speciation.Different selective pressures by the ecological niche that the organisms occupy may influence the sequence evolution of glnA1 and glnA2 and thereby affecting phylogenies based on the protein sequences they encode.

View Article: PubMed Central - HTML - PubMed

Affiliation: DST/NRF Centre for Excellence in Biomedical Tuberculosis Research, US/MRC Centre for Molecular and Cellular Biology, Division of Molecular Biology and Human Genetics, Faculty of Health Sciences - Stellenbosch University, South Africa. dh@sun.ac.za

ABSTRACT

Background: Although the gene encoding for glutamine synthetase (glnA) is essential in several organisms, multiple glnA copies have been identified in bacterial genomes such as those of the phylum Actinobacteria, notably the mycobacterial species. Intriguingly, previous reports have shown that only one copy (glnA1) is essential for growth in M. tuberculosis, while the other copies (glnA2, glnA3 and glnA4) are not.

Results: In this report it is shown that the glnA1 and glnA2 encoded glutamine synthetase sequences were inherited from an Actinobacteria ancestor, while the glnA4 and glnA3 encoded GS sequences were sequentially acquired during Actinobacteria speciation. The glutamine synthetase sequences encoded by glnA4 and glnA3 are undergoing reductive evolution in the mycobacteria, whilst those encoded by glnA1 and glnA2 are more conserved.

Conclusion: Different selective pressures by the ecological niche that the organisms occupy may influence the sequence evolution of glnA1 and glnA2 and thereby affecting phylogenies based on the protein sequences they encode. The findings in this report may impact the use of similar sequences as molecular markers, as well as shed some light on the evolution of glutamine synthetase in the mycobacteria.

Show MeSH
Related in: MedlinePlus