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Evolutionary insights about bacterial GlxRS from whole genome analyses: is GluRS2 a chimera?

Dasgupta S, Basu G - BMC Evol. Biol. (2014)

Bottom Line: Non-functional GluRS2 (as in Thermotoga maritima), on the other hand, was found to contain an anticodon-binding domain appended to a gene-duplicated catalytic domain.Several genomes were found to possess both GluRS2 and GlnRS, even though they share the common function of aminoacylating tRNAGln.The functional annotation of GluRS, without recourse to experiments, performed in this work, demonstrates the inherent and unique advantages of using whole genome over isolated sequence databases.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biophysics, Bose Institute, P-1/12 CIT Scheme VIIM, Kolkata 700054, India. gautam@boseinst.ernet.in.

ABSTRACT

Background: Evolutionary histories of glutamyl-tRNA synthetase (GluRS) and glutaminyl-tRNA synthetase (GlnRS) in bacteria are convoluted. After the divergence of eubacteria and eukarya, bacterial GluRS glutamylated both tRNAGln and tRNAGlu until GlnRS appeared by horizontal gene transfer (HGT) from eukaryotes or a duplicate copy of GluRS (GluRS2) that only glutamylates tRNAGln appeared. The current understanding is based on limited sequence data and not always compatible with available experimental results. In particular, the origin of GluRS2 is poorly understood.

Results: A large database of bacterial GluRS, GlnRS, tRNAGln and the trimeric aminoacyl-tRNA-dependent amidotransferase (gatCAB), constructed from whole genomes by functionally annotating and classifying these enzymes according to their mutual presence and absence in the genome, was analyzed. Phylogenetic analyses showed that the catalytic and the anticodon-binding domains of functional GluRS2 (as in Helicobacter pylori) were independently acquired from evolutionarily distant hosts by HGT. Non-functional GluRS2 (as in Thermotoga maritima), on the other hand, was found to contain an anticodon-binding domain appended to a gene-duplicated catalytic domain. Several genomes were found to possess both GluRS2 and GlnRS, even though they share the common function of aminoacylating tRNAGln. GlnRS was widely distributed among bacterial phyla and although phylogenetic analyses confirmed the origin of most bacterial GlnRS to be through a single HGT from eukarya, many GlnRS sequences also appeared with evolutionarily distant phyla in phylogenetic tree. A GlnRS pseudogene could be identified in Sorangium cellulosum.

Conclusions: Our analysis broadens the current understanding of bacterial GlxRS evolution and highlights the idiosyncratic evolution of GluRS2. Specifically we show that: i) GluRS2 is a chimera of mismatching catalytic and anticodon-binding domains, ii) the appearance of GlnRS and GluRS2 in a single bacterial genome indicating that the evolutionary histories of the two enzymes are distinct, iii) GlnRS is more widespread in bacteria than is believed, iv) bacterial GlnRS appeared both by HGT from eukarya and intra-bacterial HGT, v) presence of GlnRS pseudogene shows that many bacteria could not retain the newly acquired eukaryal GlnRS. The functional annotation of GluRS, without recourse to experiments, performed in this work, demonstrates the inherent and unique advantages of using whole genome over isolated sequence databases.

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Phylogeny of bacterial GluRS. Maximum Likelihood based rooted phylogenetic tree of bacterial GluRS sequences (See Methods). The functional status (see main text) of each GluRS sequences is indicated by a coloring scheme and clades are annotated by abbreviated phylum or class codes (see Table 1). Outliers (three-letter codes given Additional files 1 and 2) for panel are marked by numbers (1: NDE (ht); 2: TID (ht); 3:FMA (fi); 4: AOE (fi); 5:CTH (fi); 6: HOH (δ); 7: SSM (sp); 8: DPR (δ); 9: DPS(δ); 10: DAK (δ); 11: TGR1 (γ)). The canonical proteobacterial group is highlighted along with two groups of outlier γ- and α- proteobacterial GluRS (marked as γ* and α* and listed in Additional file 3). Branch support values < 0.7, using aLRT statistics, are indicated.
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Figure 2: Phylogeny of bacterial GluRS. Maximum Likelihood based rooted phylogenetic tree of bacterial GluRS sequences (See Methods). The functional status (see main text) of each GluRS sequences is indicated by a coloring scheme and clades are annotated by abbreviated phylum or class codes (see Table 1). Outliers (three-letter codes given Additional files 1 and 2) for panel are marked by numbers (1: NDE (ht); 2: TID (ht); 3:FMA (fi); 4: AOE (fi); 5:CTH (fi); 6: HOH (δ); 7: SSM (sp); 8: DPR (δ); 9: DPS(δ); 10: DAK (δ); 11: TGR1 (γ)). The canonical proteobacterial group is highlighted along with two groups of outlier γ- and α- proteobacterial GluRS (marked as γ* and α* and listed in Additional file 3). Branch support values < 0.7, using aLRT statistics, are indicated.

Mentions: The phylogenetic tree of representative bacterial GluRS sequences (see Additional file 3) is shown in Figure 2. The tree was constructed from all five functional flavors of GluRS described above. Except GluRS2, majority of proteobacterial GluRSs appear as a separate cluster and is farthest from the root (tenericutes/firmicutes). Non-proteobacterial GluRS also show phylum-specific clustering and the overall branching is compatible with bacterial phylogeny [21]. However, phylum-specific clustering of GluRS is not obeyed by some bacterial species. Two subgroups of γ- and α-proteobacterial GluRS sequences, marked as γ* and α* in Figure 2 and listed in Additional file 4, exhibit non-canonical behavior. These GluRS sequences appear in the non-proteobacterial cluster, as sister clades of chlamydiae, fusobacteria and deinococcous-thermus. Unlike the canonical proteobacterial GluRS (the grey shaded region of Figure 2), GluRS belonging to the γ*-/α*-group seem to have appeared through some alternate evolutionary route, probably via HGT, as has been noted earlier [22]. Interestingly, in gatB phylogeny (Figure 3) the gatB sequences of the γ*-/α*-group are not outliers, indicating that only GluRS and not gatB appeared by HGT in these bacteria. Few δ-proteobacterial GluRS (Desulfobulbus propionicus, Desulfotalea psychrophila, Desulfurivibrio alkaliphilus and Haliangium ochraceum) also appear in the non-proteobacterial clades. However, unlike the γ*-/α*-group, gatB sequences of the outlier δ-proteobacteria (in GluRS phylogeny) are also outliers in gatB phylogeny (Figure 3). This behavior could be a result of the atypical genome organizations of δ-proteobacterial species, resulting from their diverse ecologies, metabolic strategies and adaptations, which can facilitate unforeseen HGT events leading to the acquisition of both GluRS and gatB from evolutionarily distant bacterial phyla, or atypical proteins in these bacteria could have resulted from atypical evolutionary pressure [23]. Two non-proteobacterial GluRS, from hyperthermophilic bacteria (Nitrospira defluvii and Thermodesulfatator indicus), appear in the δ-proteobacterial clade. In addition, there are examples where a non-proteobacterial GluRS appears with other non-proteobacterial GluRS but not within the parent cluster. Overall, although GluRS phylogeny and the whole bacterial phylogeny are more or less consistent, Figure 2 also shows inconsistencies that could be interpreted as the result of systematic (phylum-specific) or occasional HGT among distant eubacteria.


Evolutionary insights about bacterial GlxRS from whole genome analyses: is GluRS2 a chimera?

Dasgupta S, Basu G - BMC Evol. Biol. (2014)

Phylogeny of bacterial GluRS. Maximum Likelihood based rooted phylogenetic tree of bacterial GluRS sequences (See Methods). The functional status (see main text) of each GluRS sequences is indicated by a coloring scheme and clades are annotated by abbreviated phylum or class codes (see Table 1). Outliers (three-letter codes given Additional files 1 and 2) for panel are marked by numbers (1: NDE (ht); 2: TID (ht); 3:FMA (fi); 4: AOE (fi); 5:CTH (fi); 6: HOH (δ); 7: SSM (sp); 8: DPR (δ); 9: DPS(δ); 10: DAK (δ); 11: TGR1 (γ)). The canonical proteobacterial group is highlighted along with two groups of outlier γ- and α- proteobacterial GluRS (marked as γ* and α* and listed in Additional file 3). Branch support values < 0.7, using aLRT statistics, are indicated.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC3927822&req=5

Figure 2: Phylogeny of bacterial GluRS. Maximum Likelihood based rooted phylogenetic tree of bacterial GluRS sequences (See Methods). The functional status (see main text) of each GluRS sequences is indicated by a coloring scheme and clades are annotated by abbreviated phylum or class codes (see Table 1). Outliers (three-letter codes given Additional files 1 and 2) for panel are marked by numbers (1: NDE (ht); 2: TID (ht); 3:FMA (fi); 4: AOE (fi); 5:CTH (fi); 6: HOH (δ); 7: SSM (sp); 8: DPR (δ); 9: DPS(δ); 10: DAK (δ); 11: TGR1 (γ)). The canonical proteobacterial group is highlighted along with two groups of outlier γ- and α- proteobacterial GluRS (marked as γ* and α* and listed in Additional file 3). Branch support values < 0.7, using aLRT statistics, are indicated.
Mentions: The phylogenetic tree of representative bacterial GluRS sequences (see Additional file 3) is shown in Figure 2. The tree was constructed from all five functional flavors of GluRS described above. Except GluRS2, majority of proteobacterial GluRSs appear as a separate cluster and is farthest from the root (tenericutes/firmicutes). Non-proteobacterial GluRS also show phylum-specific clustering and the overall branching is compatible with bacterial phylogeny [21]. However, phylum-specific clustering of GluRS is not obeyed by some bacterial species. Two subgroups of γ- and α-proteobacterial GluRS sequences, marked as γ* and α* in Figure 2 and listed in Additional file 4, exhibit non-canonical behavior. These GluRS sequences appear in the non-proteobacterial cluster, as sister clades of chlamydiae, fusobacteria and deinococcous-thermus. Unlike the canonical proteobacterial GluRS (the grey shaded region of Figure 2), GluRS belonging to the γ*-/α*-group seem to have appeared through some alternate evolutionary route, probably via HGT, as has been noted earlier [22]. Interestingly, in gatB phylogeny (Figure 3) the gatB sequences of the γ*-/α*-group are not outliers, indicating that only GluRS and not gatB appeared by HGT in these bacteria. Few δ-proteobacterial GluRS (Desulfobulbus propionicus, Desulfotalea psychrophila, Desulfurivibrio alkaliphilus and Haliangium ochraceum) also appear in the non-proteobacterial clades. However, unlike the γ*-/α*-group, gatB sequences of the outlier δ-proteobacteria (in GluRS phylogeny) are also outliers in gatB phylogeny (Figure 3). This behavior could be a result of the atypical genome organizations of δ-proteobacterial species, resulting from their diverse ecologies, metabolic strategies and adaptations, which can facilitate unforeseen HGT events leading to the acquisition of both GluRS and gatB from evolutionarily distant bacterial phyla, or atypical proteins in these bacteria could have resulted from atypical evolutionary pressure [23]. Two non-proteobacterial GluRS, from hyperthermophilic bacteria (Nitrospira defluvii and Thermodesulfatator indicus), appear in the δ-proteobacterial clade. In addition, there are examples where a non-proteobacterial GluRS appears with other non-proteobacterial GluRS but not within the parent cluster. Overall, although GluRS phylogeny and the whole bacterial phylogeny are more or less consistent, Figure 2 also shows inconsistencies that could be interpreted as the result of systematic (phylum-specific) or occasional HGT among distant eubacteria.

Bottom Line: Non-functional GluRS2 (as in Thermotoga maritima), on the other hand, was found to contain an anticodon-binding domain appended to a gene-duplicated catalytic domain.Several genomes were found to possess both GluRS2 and GlnRS, even though they share the common function of aminoacylating tRNAGln.The functional annotation of GluRS, without recourse to experiments, performed in this work, demonstrates the inherent and unique advantages of using whole genome over isolated sequence databases.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biophysics, Bose Institute, P-1/12 CIT Scheme VIIM, Kolkata 700054, India. gautam@boseinst.ernet.in.

ABSTRACT

Background: Evolutionary histories of glutamyl-tRNA synthetase (GluRS) and glutaminyl-tRNA synthetase (GlnRS) in bacteria are convoluted. After the divergence of eubacteria and eukarya, bacterial GluRS glutamylated both tRNAGln and tRNAGlu until GlnRS appeared by horizontal gene transfer (HGT) from eukaryotes or a duplicate copy of GluRS (GluRS2) that only glutamylates tRNAGln appeared. The current understanding is based on limited sequence data and not always compatible with available experimental results. In particular, the origin of GluRS2 is poorly understood.

Results: A large database of bacterial GluRS, GlnRS, tRNAGln and the trimeric aminoacyl-tRNA-dependent amidotransferase (gatCAB), constructed from whole genomes by functionally annotating and classifying these enzymes according to their mutual presence and absence in the genome, was analyzed. Phylogenetic analyses showed that the catalytic and the anticodon-binding domains of functional GluRS2 (as in Helicobacter pylori) were independently acquired from evolutionarily distant hosts by HGT. Non-functional GluRS2 (as in Thermotoga maritima), on the other hand, was found to contain an anticodon-binding domain appended to a gene-duplicated catalytic domain. Several genomes were found to possess both GluRS2 and GlnRS, even though they share the common function of aminoacylating tRNAGln. GlnRS was widely distributed among bacterial phyla and although phylogenetic analyses confirmed the origin of most bacterial GlnRS to be through a single HGT from eukarya, many GlnRS sequences also appeared with evolutionarily distant phyla in phylogenetic tree. A GlnRS pseudogene could be identified in Sorangium cellulosum.

Conclusions: Our analysis broadens the current understanding of bacterial GlxRS evolution and highlights the idiosyncratic evolution of GluRS2. Specifically we show that: i) GluRS2 is a chimera of mismatching catalytic and anticodon-binding domains, ii) the appearance of GlnRS and GluRS2 in a single bacterial genome indicating that the evolutionary histories of the two enzymes are distinct, iii) GlnRS is more widespread in bacteria than is believed, iv) bacterial GlnRS appeared both by HGT from eukarya and intra-bacterial HGT, v) presence of GlnRS pseudogene shows that many bacteria could not retain the newly acquired eukaryal GlnRS. The functional annotation of GluRS, without recourse to experiments, performed in this work, demonstrates the inherent and unique advantages of using whole genome over isolated sequence databases.

Show MeSH
Related in: MedlinePlus