Essentiality of threonylcarbamoyladenosine (t(6)A), a universal tRNA modification, in bacteria

Mol Microbiol. 2015 Dec;98(6):1199-221. doi: 10.1111/mmi.13209. Epub 2015 Oct 7.

Abstract

Threonylcarbamoyladenosine (t(6)A) is a modified nucleoside universally conserved in tRNAs in all three kingdoms of life. The recently discovered genes for t(6)A synthesis, including tsaC and tsaD, are essential in model prokaryotes but not essential in yeast. These genes had been identified as antibacterial targets even before their functions were known. However, the molecular basis for this prokaryotic-specific essentiality has remained a mystery. Here, we show that t(6)A is a strong positive determinant for aminoacylation of tRNA by bacterial-type but not by eukaryotic-type isoleucyl-tRNA synthetases and might also be a determinant for the essential enzyme tRNA(Ile)-lysidine synthetase. We confirm that t(6)A is essential in Escherichia coli and a survey of genome-wide essentiality studies shows that genes for t(6)A synthesis are essential in most prokaryotes. This essentiality phenotype is not universal in Bacteria as t(6)A is dispensable in Deinococcus radiodurans, Thermus thermophilus, Synechocystis PCC6803 and Streptococcus mutans. Proteomic analysis of t(6)A(-) D. radiodurans strains revealed an induction of the proteotoxic stress response and identified genes whose translation is most affected by the absence of t(6)A in tRNAs. Thus, although t(6)A is universally conserved in tRNAs, its role in translation might vary greatly between organisms.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adenosine / analogs & derivatives*
  • Adenosine / genetics
  • Adenosine / metabolism
  • Amino Acid Sequence
  • Amino Acyl-tRNA Synthetases / genetics
  • Amino Acyl-tRNA Synthetases / metabolism
  • Aminoacylation / genetics
  • Conserved Sequence
  • Deinococcus / genetics*
  • Deinococcus / metabolism
  • Escherichia coli / genetics*
  • Escherichia coli / metabolism
  • Molecular Sequence Data
  • Prokaryotic Cells
  • Proteomics
  • RNA, Bacterial / genetics
  • RNA, Bacterial / metabolism
  • RNA, Transfer / genetics*
  • RNA, Transfer / metabolism*
  • Saccharomyces cerevisiae / genetics

Substances

  • RNA, Bacterial
  • N(6)-(N-threonylcarbonyl)adenosine
  • RNA, Transfer
  • Amino Acyl-tRNA Synthetases
  • Adenosine

Associated data

  • GENBANK/BSU05910
  • GENBANK/BSU05920
  • GENBANK/BSU05940
  • GENBANK/BSU36950