Limits...
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.

Show MeSH

Related in: MedlinePlus

Phylogeny of bacterial GlnRS. Phylogenetic tree of bacterial GlnRS sequences, annotated with bacterial phyla or classes (abbreviations in Table 1). Branch support values < 0.7, calculated using aLRT statistics, are indicated. Some GlnRS sequences are highlighted based on the absence or presence of specific features in the GlnRS-containing genome: i) gatCAB-lacking genome (shown by thick lines), ii) GluRS2-containing genome, iii) genomes with Yqey-appended GlnRS, iv) genomes that contain U32-U38-A37 in their tRNAGln. Outlier GlnRS sequences (see text for details) are marked by open circles (proteobacteria) or filled boxes (non-proteobacteria). Selected clades are annotated by phylum names (see Table 1 for abbreviated phylum names).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: Phylogeny of bacterial GlnRS. Phylogenetic tree of bacterial GlnRS sequences, annotated with bacterial phyla or classes (abbreviations in Table 1). Branch support values < 0.7, calculated using aLRT statistics, are indicated. Some GlnRS sequences are highlighted based on the absence or presence of specific features in the GlnRS-containing genome: i) gatCAB-lacking genome (shown by thick lines), ii) GluRS2-containing genome, iii) genomes with Yqey-appended GlnRS, iv) genomes that contain U32-U38-A37 in their tRNAGln. Outlier GlnRS sequences (see text for details) are marked by open circles (proteobacteria) or filled boxes (non-proteobacteria). Selected clades are annotated by phylum names (see Table 1 for abbreviated phylum names).

Mentions: To gain insight about the origin of GlnRS in eubacteria, a phylogenetic tree was constructed and rooted using the sequences from firmicutes and tenericutes, as out-groups (Figure 6). Bacterial phyla with dominant presence of GlnRS (γ- and β-proteobacteria, firmicutes/tenericutes, bacteroidetes and deinococcus-thermus) cluster in a phylum-specific manner and their branching pattern in the tree is compatible with the overall bacterial phylogeny [21]. This group of GlnRS could have appeared from eukaryotic source by two different routes: i) a single HGT event, or, ii) phylum-specific multiple HGT events. While the second route cannot be ruled out, the overall compatibility of GlnRS phylogeny and bacterial phylogeny suggests that there was a single, and not multiple HGT events, that resulted in the acquisition of eukaryotic GlnRS by bacterium. Subsequently, as bacteria diverged, so did GlnRS, but it could be retained only by some bacterial phyla. Factors that may have played a role in the retention of GlnRS are discussed later.


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

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

Phylogeny of bacterial GlnRS. Phylogenetic tree of bacterial GlnRS sequences, annotated with bacterial phyla or classes (abbreviations in Table 1). Branch support values < 0.7, calculated using aLRT statistics, are indicated. Some GlnRS sequences are highlighted based on the absence or presence of specific features in the GlnRS-containing genome: i) gatCAB-lacking genome (shown by thick lines), ii) GluRS2-containing genome, iii) genomes with Yqey-appended GlnRS, iv) genomes that contain U32-U38-A37 in their tRNAGln. Outlier GlnRS sequences (see text for details) are marked by open circles (proteobacteria) or filled boxes (non-proteobacteria). Selected clades are annotated by phylum names (see Table 1 for abbreviated phylum names).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: Phylogeny of bacterial GlnRS. Phylogenetic tree of bacterial GlnRS sequences, annotated with bacterial phyla or classes (abbreviations in Table 1). Branch support values < 0.7, calculated using aLRT statistics, are indicated. Some GlnRS sequences are highlighted based on the absence or presence of specific features in the GlnRS-containing genome: i) gatCAB-lacking genome (shown by thick lines), ii) GluRS2-containing genome, iii) genomes with Yqey-appended GlnRS, iv) genomes that contain U32-U38-A37 in their tRNAGln. Outlier GlnRS sequences (see text for details) are marked by open circles (proteobacteria) or filled boxes (non-proteobacteria). Selected clades are annotated by phylum names (see Table 1 for abbreviated phylum names).
Mentions: To gain insight about the origin of GlnRS in eubacteria, a phylogenetic tree was constructed and rooted using the sequences from firmicutes and tenericutes, as out-groups (Figure 6). Bacterial phyla with dominant presence of GlnRS (γ- and β-proteobacteria, firmicutes/tenericutes, bacteroidetes and deinococcus-thermus) cluster in a phylum-specific manner and their branching pattern in the tree is compatible with the overall bacterial phylogeny [21]. This group of GlnRS could have appeared from eukaryotic source by two different routes: i) a single HGT event, or, ii) phylum-specific multiple HGT events. While the second route cannot be ruled out, the overall compatibility of GlnRS phylogeny and bacterial phylogeny suggests that there was a single, and not multiple HGT events, that resulted in the acquisition of eukaryotic GlnRS by bacterium. Subsequently, as bacteria diverged, so did GlnRS, but it could be retained only by some bacterial phyla. Factors that may have played a role in the retention of GlnRS are discussed later.

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