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Review
. 2019 Mar 8:10:204.
doi: 10.3389/fgene.2019.00204. eCollection 2019.

Regulatory Factors for tRNA Modifications in Extreme- Thermophilic Bacterium Thermus thermophilus

Hiroyuki Hori  1
Affiliations
Review

Regulatory Factors for tRNA Modifications in Extreme- Thermophilic Bacterium Thermus thermophilus

Hiroyuki Hori. Front Genet. .

Abstract

Thermus thermophilus is an extreme-thermophilic bacterium that can grow at a wide range of temperatures (50-83°C). To enable T. thermophilus to grow at high temperatures, several biomolecules including tRNA and tRNA modification enzymes show extreme heat-resistance. Therefore, the modified nucleosides in tRNA from T. thermophilus have been studied mainly from the view point of tRNA stabilization at high temperatures. Such studies have shown that several modifications stabilize the structure of tRNA and are essential for survival of the organism at high temperatures. Together with tRNA modification enzymes, the modified nucleosides form a network that regulates the extent of different tRNA modifications at various temperatures. In this review, I describe this network, as well as the tRNA recognition mechanism of individual tRNA modification enzymes. Furthermore, I summarize the roles of other tRNA stabilization factors such as polyamines and metal ions.

Keywords: RNA modification; Thermus thermophilus; methylation; tRNA; thermophile.

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Figures

FIGURE 1
FIGURE 1
Cloverleaf representation of Thermus thermophilus tRNAPhe. Modified nucleosides are colored in red and numbers indicate the modification positions. Parentheses indicate that the modification is partial. The abbreviations of modified nucleosides are given in Table 1.
FIGURE 2
FIGURE 2
Structures of modified nucleosides in T. thermophilus tRNAPhe. The modifications are highlighted in red. Because ψ is synthesized by isomerization of uridine, the base is enclosed by a red circle.
FIGURE 3
FIGURE 3
Extents of m7G46, m1A58, Gm18, and m5s2U54 modifications in tRNAPhe from T. thermophilus. The extent of m7G46, m1A58, and Gm18 modifications was measured by a methylation assay with TrmB, TrmI, and TrmH, respectively. The extent of m5s2U54 modification was estimated from the peak areas of m5U54 and m5s2U54 on HPLC analysis. This figure is prepared from Figure 3 in a chapter “Regulation of Protein Synthesis via the Network Between Modified Nucleotides in tRNA and tRNA Modification Enzymes in T. thermophilus, a Thermophilic Eubacterium” of a book “Modified Nucleic Acids in Biology and Medicine,” Springer Nature 2016 with permission (4517441319562) from the publisher.
FIGURE 4
FIGURE 4
Minimum substrate RNA or positive determinants for tRNA modification enzymes. (A) TrmFO; (B), TtuA; (C), TrmI; (D), TruB; (E), TrmB; (F) TrmH; (G) ThiI. The modification is indicated in parentheses; the modification site is colored in red. See the main text for details.
FIGURE 5
FIGURE 5
TrmH and the pre-steady state analysis of complex formation between TrmH and tRNA. (A) Dimer structure of TrmH. AdoMet, Arg41 and tryptophan residues are highlighted by stick-models. The two subunits of TrmH are distinguished by green and blue coloring. Trp126 residue is located near AdoMet in the blue subunit and Arg41 in the green subunit. (B) Stopped-flow fluorescence measurement of TrmH–tRNA complex formation. See main text for details.
FIGURE 6
FIGURE 6
Network between modified nucleosides in tRNA and tRNA modification enzymes in T. thermophilus. (A) Network at high temperatures (>75°C). The m7G46 modification (highlighted in red) is a key factor in this network. Its presence accelerates the speed of other tRNA modification enzymes such as TrmH, TrmD, and TrmI. In addition, the presence of m5U54 also increases the methylation speed of TrmI. The increase in m1A58 due to accelerated TrmI activity further increases the speed of sulfur-transfer by TtuA and that of related proteins, and results in an increased percentage of m5s2U54. The introduced modifications coordinately stabilize the L-shaped tRNA structure. (B) Network at low temperatures (<55°C). In this network, the ψ55 modification stabilizes the local structure in tRNA and slows down the speed of tRNA modification enzymes. The m5U54 modification plays a role in maintaining the balance of modifications at the elbow region in tRNA. This figure is prepared from Figure 4 in a chapter “Regulation of Protein Synthesis via the Network Between Modified Nucleotides in tRNA and tRNA Modification Enzymes in T. thermophilus, a Thermophilic Eubacterium” of a book “Modified Nucleic Acids in Biology and Medicine” Springer Nature 2016 with permission (4517441319562) from the publisher.
FIGURE 7
FIGURE 7
Effect of polyamines on TrmH activity. (A) Typical polyamines. Putrescine, spermidine, and spermine are the three standard polyamines that are found in all living organisms. Unique long and branched polyamines such as caldohexamine and tetrakis(3-aminopropyl)ammonium (Taa) exist in T. thermophilus. (B) TrmH activity was measured in the presence (blue filled circles) or absence (black open circles) of polyamines at 40–90°C. Only in the presence of appropriate concentrations of caldohexamine (1.5 mM) or Taa (0.25 mM), T. thermophilus TrmH can methylate yeast tRNAPhe transcript, of which the melting temperature is 69°C, at 80°C (red arrow).
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References

    1. Agarwalla S., Kealey J. T., Santi D. V., Stroud R. M. (2002). Characterization of the 23 S ribosomal RNA m5U1939 methyltransferase from Escherichia coli. J. Biol. Chem. 277 8835–8840. 10.1074/jbc.M111825200 - DOI - PubMed
    1. Agris P. F. (1996). The importance of being modified: roles of modified nucleosides and Mg2+ in RNA structure and function. Prog. Nucleic Acid Res. Mol. Biol. 53 79–129. 10.1016/S0079-6603(08)60143-9 - DOI - PubMed
    1. Agris P. F., Eruysal E. R., Narendran A., Väre V. Y. P., Vangaveti S., Ranganathan S. V. (2018). Celebrating wobble decoding: half a century and still much is new. RNA Biol. 15 537–553. 10.1080/15476286.2017.1356562 - DOI - PMC - PubMed
    1. Anantharaman V., Koonin E. V., Aravind L. (2002). SPOUT: a class of methyltransferases that includes spoU and trmD RNA methylase superfamilies, and novel superfamilies of predicted prokaryotic RNA methylases. J. Mol. Microbiol. Biotechnol. 4 71–75. - PubMed
    1. Armengod M. E., Meseguer S., Villarroya M., Prado S., Moukadiri I., Ruiz-Partida R., et al. (2014). Modification of the wobble uridine in bacterial and mitochondrial tRNAs reading NNA/NNG triplets of 2-codon boxes. RNA Biol. 11 1495–1507. 10.4161/15476286.2014.992269 - DOI - PMC - PubMed

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