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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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Evolutionary model of bacterial and eukaryal GlxRS. The N-terminal catalytic and the C-terminal anticodon-binding domains of GlxRS are annotated by the letters N and C, and depicted according to their mutual homology (oval: N-terminal domains of all GluRS and GlnRS; diamond: C-terminal domains of all GlnRS and eukaryal GluRS; square: C-terminal domains of bacterial GluRS). tRNAGlx-aminocylation specificities of GlxRS are indicated by color-coded shades. HGT and ‘?’ stand for horizontal gene transfer and ‘open questions’, respectively.
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Figure 1: Evolutionary model of bacterial and eukaryal GlxRS. The N-terminal catalytic and the C-terminal anticodon-binding domains of GlxRS are annotated by the letters N and C, and depicted according to their mutual homology (oval: N-terminal domains of all GluRS and GlnRS; diamond: C-terminal domains of all GlnRS and eukaryal GluRS; square: C-terminal domains of bacterial GluRS). tRNAGlx-aminocylation specificities of GlxRS are indicated by color-coded shades. HGT and ‘?’ stand for horizontal gene transfer and ‘open questions’, respectively.

Mentions: Although extant GluRS (and GlnRS) is a two-domain protein consisting of a N-terminal catalytic domain and a C-terminal anticodon-binding domain, the C-terminal anticodon-binding domain was added to the catalytic domain only after bacteria and eukaryotes diverged [7-9]. This is reflected in the fact that the anticodon-binding domains of bacterial and eukaryotic GluRS, although functionally similar, are structurally very different (See Figure 1) [10]. GluRS is also considered to be more ancient than GlnRS. GlnRS appeared first in eukaryotes, by gene duplication of GluRS followed by selective amino acid modifications. This is supported by the observation that eukaryotic GluRS and GlnRS in eukaryotes are structurally very similar [11]. However, the same is not true for bacterial GlnRS and GluRS. The anticodon-binding domain of bacterial GlnRS is structurally homologous to eukaryotic GlnRS rather than to bacterial GluRS. Based on this, it has been hypothesized that bacteria acquired GlnRS from eukaryotes by HGT [7,12]. The evolutionary origin of bacterial GluRS2 is not so clear with suggestions that it evolved either from the canonical GluRS/GluRS1 by gene duplication [5] or it appeared in bacteria by HGT [13].


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

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

Evolutionary model of bacterial and eukaryal GlxRS. The N-terminal catalytic and the C-terminal anticodon-binding domains of GlxRS are annotated by the letters N and C, and depicted according to their mutual homology (oval: N-terminal domains of all GluRS and GlnRS; diamond: C-terminal domains of all GlnRS and eukaryal GluRS; square: C-terminal domains of bacterial GluRS). tRNAGlx-aminocylation specificities of GlxRS are indicated by color-coded shades. HGT and ‘?’ stand for horizontal gene transfer and ‘open questions’, respectively.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Evolutionary model of bacterial and eukaryal GlxRS. The N-terminal catalytic and the C-terminal anticodon-binding domains of GlxRS are annotated by the letters N and C, and depicted according to their mutual homology (oval: N-terminal domains of all GluRS and GlnRS; diamond: C-terminal domains of all GlnRS and eukaryal GluRS; square: C-terminal domains of bacterial GluRS). tRNAGlx-aminocylation specificities of GlxRS are indicated by color-coded shades. HGT and ‘?’ stand for horizontal gene transfer and ‘open questions’, respectively.
Mentions: Although extant GluRS (and GlnRS) is a two-domain protein consisting of a N-terminal catalytic domain and a C-terminal anticodon-binding domain, the C-terminal anticodon-binding domain was added to the catalytic domain only after bacteria and eukaryotes diverged [7-9]. This is reflected in the fact that the anticodon-binding domains of bacterial and eukaryotic GluRS, although functionally similar, are structurally very different (See Figure 1) [10]. GluRS is also considered to be more ancient than GlnRS. GlnRS appeared first in eukaryotes, by gene duplication of GluRS followed by selective amino acid modifications. This is supported by the observation that eukaryotic GluRS and GlnRS in eukaryotes are structurally very similar [11]. However, the same is not true for bacterial GlnRS and GluRS. The anticodon-binding domain of bacterial GlnRS is structurally homologous to eukaryotic GlnRS rather than to bacterial GluRS. Based on this, it has been hypothesized that bacteria acquired GlnRS from eukaryotes by HGT [7,12]. The evolutionary origin of bacterial GluRS2 is not so clear with suggestions that it evolved either from the canonical GluRS/GluRS1 by gene duplication [5] or it appeared in bacteria by HGT [13].

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