Transfer-messenger RNA controls the translation of cell-cycle and stress proteins in Streptomyces.
The transfer-messenger RNA (tmRNA)-mediated trans-translation mechanism is highly conserved in bacteria and functions primarily as a system for the rescue of stalled ribosomes and the removal of aberrantly produced proteins. Here, we show that in the antibiotic-producing soil bacterium Streptomyces coelicolor, trans-translation has a specialized role in stress management. Analysis of proteins that were carboxy-terminally His(8)-tagged by a recombinant tmRNA identified only 10 targets, including the stress proteins: DnaK heat-shock protein 70, thiostrepton-induced protein A, universal stress protein A, elongation factor Tu3, and the cell-cycle control proteins DasR, SsgA, SsgF and SsgR. Although tmRNA-tagged proteins are degraded swiftly, the translation of dnaK and dasR messenger RNAs (mRNAs) depends fully on tmRNA, whereas transcription is unaffected. The data unveil a surprisingly dedicated functionality for tmRNA, promoting the translation of the same mRNA it targets, at the expense of sacrificing the first nascent protein. In streptomycetes, tmRNA has evolved into a dedicated task force that ensures the instantaneous response to the exposure to stress.
Barends
Sharief
S
Microbial Development, Leiden Institute of Chemistry, Leiden University, Einsteinweg 55, 2333 CC, Leiden, The Netherlands.
Zehl
Martin
M
Bialek
Sylwia
S
de Waal
Ellen
E
Traag
Bjørn A
BA
Willemse
Joost
J
Jensen
Ole Nørregaard
ON
Vijgenboom
Erik
E
van Wezel
Gilles P
GP
D001426:Bacterial Proteins / Q000032:analysis / Q000378:metabolism; D018797:Cell Cycle Proteins / Q000378:metabolism*; D006360:Heat-Shock Proteins / Q000378:metabolism*; D008954:Models, Biological; D014176:Protein Biosynthesis / Q000235:genetics*; D020543:Proteome / Q000032:analysis / Q000378:metabolism; D012333:RNA, Messenger / Q000502:physiology*; D012343:RNA, Transfer / Q000502:physiology*; D048372:Streptomyces coelicolor / Q000235:genetics / Q000378:metabolism*
D001426:Bacterial Proteins; D018797:Cell Cycle Proteins; D006360:Heat-Shock Proteins; D020543:Proteome; D012333:RNA, Messenger; D012343:RNA, Transfer