Survival of mycobacteria depends on proteasome-mediated amino acid recycling under nutrient limitation

EMBO J. 2014 Aug 18;33(16):1802-14. doi: 10.15252/embj.201387076. Epub 2014 Jul 1.

Abstract

Intracellular protein degradation is an essential process in all life domains. While in all eukaryotes regulated protein degradation involves ubiquitin tagging and the 26S-proteasome, bacterial prokaryotic ubiquitin-like protein (Pup) tagging and proteasomes are conserved only in species belonging to the phyla Actinobacteria and Nitrospira. In Mycobacterium tuberculosis, the Pup-proteasome system (PPS) is important for virulence, yet its physiological role in non-pathogenic species has remained an enigma. We now report, using Mycobacterium smegmatis as a model organism, that the PPS is essential for survival under starvation. Upon nitrogen limitation, PPS activity is induced, leading to accelerated tagging and degradation of many cytoplasmic proteins. We suggest a model in which the PPS functions to recycle amino acids under nitrogen starvation, thereby enabling the cell to maintain basal metabolic activities. We also find that the PPS auto-regulates its own activity via pupylation and degradation of its components in a manner that promotes the oscillatory expression of PPS components. As such, the destructive activity of the PPS is carefully balanced to maintain cellular functions during starvation.

Keywords: mycobacteria; nitrogen limitation; proteasome; proteolysis; pupylation.

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Amino Acids / metabolism*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Carbon / metabolism
  • Gene Expression Regulation, Bacterial
  • Homeostasis
  • Mutation
  • Mycobacterium smegmatis / growth & development
  • Mycobacterium smegmatis / metabolism*
  • Mycobacterium smegmatis / physiology
  • Nitrogen / metabolism
  • Operon
  • Proteasome Endopeptidase Complex / genetics
  • Proteasome Endopeptidase Complex / metabolism*
  • Proteolysis

Substances

  • Amino Acids
  • Bacterial Proteins
  • Carbon
  • Adenosine Triphosphate
  • Proteasome Endopeptidase Complex
  • Nitrogen