Phylogeny and Evolution of RNA 3′-Nucleotidyltransferases in Bacteria

Jones, George H.

doi:10.1007/s00239-019-09907-2

Cited by 4 publications

(29 citation statements)

References 59 publications

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“…While the chimera readily incorporated two C-residues on a tRNA substrate, it completely failed to add the terminal A ( Figure S2). This result corroborates our previous findings that only loop sequences of evolutionary closely related enzymes are compatible, while the corresponding region from distantly related enzymes are not exchangeable [22,24,25,33]. .…”

Section: Schizosaccharomyces Pombe Has Two Ancestral Eukaryotic Nuclesupporting

confidence: 92%

“…Hence, it is possible that other enzyme parts important for A-addition are also affected in the CC-adding enzymes. Besides the B/A motif and the flexible loop, a springy hinge region consisting of interacting α-helical elements located in motif C helps to define the number of nucleotides to be incorporated and contributes to the structural rearrangements of the NTP binding pocket, although no direct interaction with the loop region could be demonstrated [24,33,58]. As the sequence variation of this motif between CC-and CCA-adding enzymes is identical to that found within the CCA-adding enzymes, it is highly unlikely that motif C mutations are responsible for the restricted activity of the investigated CC-adding enzymes.…”

Section: The Flexible Loop-equally Important For the Evolution Of Cc-mentioning

confidence: 99%

“…Due to its flexibility, the loop region is disordered and not resolved in most of the crystal structures of class II CCA-adding enzymes. Based on structural models of this region, it was suggested that the deviating loop sequence in the S. pombe CC-adding enzyme forms a short β-sheet that restricts its flexibility and, as a consequence, inhibits A-addition [33,37]. In the crystal structure of the T. maritima enzyme, however, the loop structure is resolved and also folds into the short β-sheet [24].…”

Section: The Flexible Loop-equally Important For the Evolution Of Cc-mentioning

confidence: 99%

“…While both types of enzymes share the five core motifs with class II CCA-adding enzymes, the flexible loop region is absent in CC-adding enzymes, inhibiting the switch from CTP to ATP specificity. This deletion suggests that bacterial CC-adding enzymes originated from CCA-adding enzymes [22,33]. In A-adding enzymes, on the other hand, the structure of the C-terminal part (located outside of the catalytic core) is equipped with a physical constraint that prevents short tRNAs without a 3 CC end from entering the catalytic core for A-addition [32,34].…”

Section: Introductionmentioning

confidence: 99%

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Divergent Evolution of Eukaryotic CC- and A-Adding Enzymes

Erber

Franz

Betat

et al. 2020

IJMS

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Synthesis of the CCA end of essential tRNAs is performed either by CCA-adding enzymes or as a collaboration between enzymes restricted to CC- and A-incorporation. While the occurrence of such tRNA nucleotidyltransferases with partial activities seemed to be restricted to Bacteria, the first example of such split CCA-adding activities was reported in Schizosaccharomyces pombe. Here, we demonstrate that the choanoflagellate Salpingoeca rosetta also carries CC- and A-adding enzymes. However, these enzymes have distinct evolutionary origins. Furthermore, the restricted activity of the eukaryotic CC-adding enzymes has evolved in a different way compared to their bacterial counterparts. Yet, the molecular basis is very similar, as highly conserved positions within a catalytically important flexible loop region are missing in the CC-adding enzymes. For both the CC-adding enzymes from S. rosetta as well as S. pombe, introduction of the loop elements from closely related enzymes with full activity was able to restore CCA-addition, corroborating the significance of this loop in the evolution of bacterial as well as eukaryotic tRNA nucleotidyltransferases. Our data demonstrate that partial CC- and A-adding activities in Bacteria and Eukaryotes are based on the same mechanistic principles but, surprisingly, originate from different evolutionary events.

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Section: Schizosaccharomyces Pombe Has Two Ancestral Eukaryotic Nuclesupporting

confidence: 92%

Section: The Flexible Loop-equally Important For the Evolution Of Cc-mentioning

confidence: 99%

Section: The Flexible Loop-equally Important For the Evolution Of Cc-mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Divergent Evolution of Eukaryotic CC- and A-Adding Enzymes

Erber

Franz

Betat

et al. 2020

IJMS

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“…Alien indices, indicative of the likelihood of horizontal transfer of pcnB genes from the donor to the recipient species listed in Table 1, were calculated as described previously [1,28]. Details of the calculations are provided in Results and Discussion.…”

Section: Alien Index and G+c Content Calculationsmentioning

confidence: 99%

Acquisition of pcnB [poly(A) polymerase I] genes via horizontal transfer from the β, γ-Proteobacteria

Jones

2021

Microbial Genomics

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Poly(A) polymerases (PAPs) and tRNA nucleotidyltransferases belong to a superfamily of nucleotidyltransferases and modify RNA 3′-ends. The product of the pcnB gene, PAP I, has been characterized in a few β-, γ- and δ- Proteobacteria . Using the PAP I signature sequence, putative PAPs were identified in bacterial species from the α- and ε- Proteobacteria and from four other bacterial phyla ( Firmicutes , Actinobacteria , Bacteroidetes and Aquificae ). Phylogenetic analysis, alien index and G+C content calculations strongly suggest that the PAPs in the species identified in this study arose by horizontal gene transfer from the β- and γ- Proteobacteria .

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CCA-Addition Gone Wild: Unusual Occurrence and Phylogeny of Four Different tRNA Nucleotidyltransferases in Acanthamoeba castellanii

Erber

Betat

Mörl

2020

Molecular Biology and Evolution

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tRNAs are important players in the protein synthesis machinery, where they act as adapter molecules for translating the mRNA codons into the corresponding amino acid sequence. In a series of highly conserved maturation steps, the primary transcripts are converted into mature tRNAs. In the amoebozoan Acanthamoeba castellanii, a highly unusual evolution of some of these processing steps was identified that are based on unconventional RNA polymerase activities. In this context, we investigated the synthesis of the 3’-terminal CCA-end that is added posttranscriptionally by a specialized polymerase, the tRNA nucleotidyltransferase (CCA-adding enzyme). The majority of eukaryotic organisms carry only a single gene for a CCA-adding enzyme that acts on both the cytosolic as well as the mitochondrial tRNA pool. In a bioinformatic analysis of the genome of this organism, we identified a surprising multitude of genes for enzymes that contain the active site signature of eukaryotic/eubacterial tRNA nucleotidyltransferases. In vitro activity analyses of these enzymes revealed that two proteins represent bona fide CCA-adding enzymes, one of them carrying an N-terminal sequence corresponding to a putative mitochondrial target signal. The other enzymes have restricted activities and represent CC- and A-adding enzymes, respectively. The A–adding enzyme is of particular interest, as its sequence is closely related to corresponding enzymes from Proteobacteria, indicating a horizontal gene transfer. Interestingly, this unusual diversity of nucleotidyltransferase genes is not restricted to A. castellanii, but is also present in other members of the Acanthamoeba genus, indicating an ancient evolutionary trait.

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Phylogeny and Evolution of RNA 3′-Nucleotidyltransferases in Bacteria

Cited by 4 publications

References 59 publications

Divergent Evolution of Eukaryotic CC- and A-Adding Enzymes

Divergent Evolution of Eukaryotic CC- and A-Adding Enzymes

Acquisition of pcnB [poly(A) polymerase I] genes via horizontal transfer from the β, γ-Proteobacteria

CCA-Addition Gone Wild: Unusual Occurrence and Phylogeny of Four Different tRNA Nucleotidyltransferases in Acanthamoeba castellanii

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