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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 N-terminal catalytic and the C-terminal anticodon-binding domains of bacterial GluRS. All annotations marking the trees are consistent with Figure¬†2. Branch support values‚ÄČ<‚ÄČ0.7, using aLRT statistics, are indicated. The structure shown on the left corresponds to the crystal structure of T. thermophilus GluRS (pdb ID: 1j09) with residues 1-322 and 323-468 comprising the N- and the C-terminal domains, respectively.
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Figure 4: Phylogeny of N-terminal catalytic and the C-terminal anticodon-binding domains of bacterial GluRS. All annotations marking the trees are consistent with Figure¬†2. Branch support values‚ÄČ<‚ÄČ0.7, using aLRT statistics, are indicated. The structure shown on the left corresponds to the crystal structure of T. thermophilus GluRS (pdb ID: 1j09) with residues 1-322 and 323-468 comprising the N- and the C-terminal domains, respectively.

Mentions: It is thought that the primordial GluRS consisted of only the N-terminal catalytic domain (GluRS(N)). Later, during the course of evolution, the C-terminal domain (GluRS(C)) was appended to it [7,12]. As a consequence, the two domains may not display identical branching patterns in phylogenetic trees constructed independently from the two isolated domains. Indeed, a comparison of GluRS(N) and GluRS(C) phylogenies (upper and lowers panels in Figure 4) showed that except for the canonical proteobacterial GluRS group (containing GluRS and GluRS1), the GluRS(N)- and GluRS(C)-derived cladograms are not strictly mirror images of each other. One reason for this observation could be that GluRS(C) was appended after the phylum-specific divergence of GluRS(N) in bacteria. However, according to this model different bacterial phyla acquired different GluRS(C) independently, which is a very unlikely event. A more realistic model is where GluRS(C) was appended to GluRS(N) before bacterial phylum-divergence but because the acquired GluRS(C) was non-functional, it was lost and regained several times, probably via intra-bacterial HGT, before becoming functionally compatible with GluRS(N) in a synchronous way [26,27]. This model is compatible with Figure 4. In other words, GluRS(C) is more mobile than GluRS(N) and is prone to frequent intra-bacterial HGT. Figure 4 also suggests that GluRS(N) is the core functional domain of GluRS, since the branching topology of GluRS(N) phylogeny (upper panel of Figure 4), but not GluRS(C) phylogeny (lower panel of Figure 4), is compatible with the overall bacterial phylogeny [21].


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

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

Phylogeny of N-terminal catalytic and the C-terminal anticodon-binding domains of bacterial GluRS. All annotations marking the trees are consistent with Figure¬†2. Branch support values‚ÄČ<‚ÄČ0.7, using aLRT statistics, are indicated. The structure shown on the left corresponds to the crystal structure of T. thermophilus GluRS (pdb ID: 1j09) with residues 1-322 and 323-468 comprising the N- and the C-terminal domains, respectively.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Phylogeny of N-terminal catalytic and the C-terminal anticodon-binding domains of bacterial GluRS. All annotations marking the trees are consistent with Figure¬†2. Branch support values‚ÄČ<‚ÄČ0.7, using aLRT statistics, are indicated. The structure shown on the left corresponds to the crystal structure of T. thermophilus GluRS (pdb ID: 1j09) with residues 1-322 and 323-468 comprising the N- and the C-terminal domains, respectively.
Mentions: It is thought that the primordial GluRS consisted of only the N-terminal catalytic domain (GluRS(N)). Later, during the course of evolution, the C-terminal domain (GluRS(C)) was appended to it [7,12]. As a consequence, the two domains may not display identical branching patterns in phylogenetic trees constructed independently from the two isolated domains. Indeed, a comparison of GluRS(N) and GluRS(C) phylogenies (upper and lowers panels in Figure 4) showed that except for the canonical proteobacterial GluRS group (containing GluRS and GluRS1), the GluRS(N)- and GluRS(C)-derived cladograms are not strictly mirror images of each other. One reason for this observation could be that GluRS(C) was appended after the phylum-specific divergence of GluRS(N) in bacteria. However, according to this model different bacterial phyla acquired different GluRS(C) independently, which is a very unlikely event. A more realistic model is where GluRS(C) was appended to GluRS(N) before bacterial phylum-divergence but because the acquired GluRS(C) was non-functional, it was lost and regained several times, probably via intra-bacterial HGT, before becoming functionally compatible with GluRS(N) in a synchronous way [26,27]. This model is compatible with Figure 4. In other words, GluRS(C) is more mobile than GluRS(N) and is prone to frequent intra-bacterial HGT. Figure 4 also suggests that GluRS(N) is the core functional domain of GluRS, since the branching topology of GluRS(N) phylogeny (upper panel of Figure 4), but not GluRS(C) phylogeny (lower panel of Figure 4), is compatible with the overall bacterial phylogeny [21].

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