Abstract

Translational systems can respond promptly to sudden environmental changes to provide rapid adaptations to environmental stress. Unlike the well-studied translational responses to oxidative stress in eukaryotic systems, little is known regarding how prokaryotes respond rapidly to oxidative stress in terms of translation. In this study, we measured protein synthesis from the entire Escherichia coli proteome and found that protein synthesis was severely slowed down under oxidative stress. With unchanged translation initiation, this slowdown was caused by decreased translation elongation speed. We further confirmed by tRNA sequencing and qRT-PCR that this deceleration was caused by a global, enzymatic downregulation of almost all tRNA species shortly after exposure to oxidative agents. Elevation in tRNA levels accelerated translation and protected E. coli against oxidative stress caused by hydrogen peroxide and the antibiotic ciprofloxacin. Our results showed that the global regulation of tRNAs mediates the rapid adjustment of the E. coli translation system for prompt adaptation to oxidative stress.

Highlights

  • Reactive oxygen species (ROS), such as hydrogen peroxide (H2O2), the hydroxyl radical (ÁOH), and superoxide (O2-), are mainly generated as byproducts of the respiratory chain or introduced on exposure to a hazardous environment [1]

  • Translational regulation can occur in response to environmental stresses within minutes, which is much faster than transcriptional regulation, and normally provides immediate adaptation

  • We showed for the first time that bacteria respond to oxidative stress by adjusting the translational system in a manner that differs from that of eukaryotes

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Summary

Introduction

Reactive oxygen species (ROS), such as hydrogen peroxide (H2O2), the hydroxyl radical (ÁOH), and superoxide (O2-), are mainly generated as byproducts of the respiratory chain or introduced on exposure to a hazardous environment [1] These ROSs can damage proteins and nucleic acids by oxidation, leading to cellular oxidative stress (reviewed in [1,2,3]). Studies suggested that translation is globally inhibited in 5 min in Saccharomyces cerevisiae cells [8]. This process is mediated by specific tRNA and rRNA cleavage [9,10]. The tRNALeu(CAA) hypermodified at the wobble position increases the translation of TTG codons after H2O2 exposure and enhanced the protein expression of TTG-enriched genes [17]

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