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A new family of bacterial ribosome hibernation factors.

Karla Helena-BuenoMariia Yu RybakChinenye L EkemezieRudi SullivanCharlotte R BrownCharlotte DingwallArnaud BasléClaudia SchneiderJames P R ConnollyJames N BlazaBálint CsörgőPatrick Joseph MoynihanMatthieu G GagnonChris H HillSergey V Melnikov
Published in: Nature (2024)
To conserve energy during starvation and stress, many organisms use hibernation factor proteins to inhibit protein synthesis and protect their ribosomes from damage 1,2 . In bacteria, two families of hibernation factors have been described, but the low conservation of these proteins and the huge diversity of species, habitats and environmental stressors have confounded their discovery 3-6 . Here, by combining cryogenic electron microscopy, genetics and biochemistry, we identify Balon, a new hibernation factor in the cold-adapted bacterium Psychrobacter urativorans. We show that Balon is a distant homologue of the archaeo-eukaryotic translation factor aeRF1 and is found in 20% of representative bacteria. During cold shock or stationary phase, Balon occupies the ribosomal A site in both vacant and actively translating ribosomes in complex with EF-Tu, highlighting an unexpected role for EF-Tu in the cellular stress response. Unlike typical A-site substrates, Balon binds to ribosomes in an mRNA-independent manner, initiating a new mode of ribosome hibernation that can commence while ribosomes are still engaged in protein synthesis. Our work suggests that Balon-EF-Tu-regulated ribosome hibernation is a ubiquitous bacterial stress-response mechanism, and we demonstrate that putative Balon homologues in Mycobacteria bind to ribosomes in a similar fashion. This finding calls for a revision of the current model of ribosome hibernation inferred from common model organisms and holds numerous implications for how we understand and study ribosome hibernation.
Keyphrases
  • electron microscopy
  • oxidative stress
  • small molecule
  • gram negative
  • transcription factor
  • cross sectional
  • high throughput
  • heat stress
  • mass spectrometry
  • single cell
  • emergency medical