Functional association of the stress-responsive LiaH protein and the minimal TatAyCy protein translocase in Bacillus subtilis

Research output: Contribution to journalResearch articleContributedpeer-review

Contributors

  • Margarita Bernal-Cabas - , University of Groningen (Author)
  • Marcus Miethke - , University of Groningen (Author)
  • Minia Antelo-Varela - , University of Greifswald (Author)
  • Rocío Aguilar Suárez - , University of Groningen (Author)
  • Jolanda Neef - , University of Groningen (Author)
  • Larissa Schön - , University of Groningen (Author)
  • Giorgio Gabarrini - , University of Groningen (Author)
  • Andreas Otto - , Institute of Microbiology, Chair of Pavement Engineering, University of Greifswald (Author)
  • Dörte Becher - , University of Greifswald (Author)
  • Diana Wolf - , Institute of Microbiology, Chair of General Microbiology (Author)
  • Jan Maarten van Dijl - , University of Groningen (Author)

Abstract

The bacterial twin-arginine (Tat) pathway serves in the exclusive secretion of folded proteins with bound cofactors. While Tat pathways in Gram-negative bacteria and chloroplast thylakoids consist of conserved TatA, TatB and TatC subunits, the Tat pathways of Bacillus species and many other Gram-positive bacteria stand out for their minimalist nature with the core translocase being composed of essential TatA and TatC subunits only. Here we addressed the question whether the minimal TatAyCy translocase of Bacillus subtilis recruits additional cellular components that modulate its activity. To this end, TatAyCy was purified by affinity- and size exclusion chromatography, and interacting co-purified proteins were identified by mass spectrometry. This uncovered the cell envelope stress responsive LiaH protein as an accessory subunit of the TatAyCy complex. Importantly, our functional studies show that Tat expression is tightly trailed by LiaH induction, and that LiaH itself determines the capacity and quality of TatAyCy-dependent protein translocation. In contrast, LiaH has no role in high-level protein secretion via the general secretion (Sec) pathway. Altogether, our observations show that protein translocation by the minimal Tat translocase TatAyCy is tightly intertwined with an adequate bacterial response to cell envelope stress. This is consistent with a critical need to maintain cellular homeostasis, especially when the membrane is widely opened to permit passage of large fully-folded proteins via Tat.

Details

Original languageEnglish
Pages (from-to)118719
JournalBiochimica et biophysica acta. Molecular cell research
Volume1867
Issue number8
Publication statusPublished - Aug 2020
Peer-reviewedYes

External IDs

Scopus 85083437423

Keywords

Keywords

  • Bacillus subtilis/enzymology, Bacterial Proteins/genetics, Carrier Proteins/metabolism, Cell Membrane/metabolism, Escherichia coli/enzymology, Escherichia coli Proteins, Gene Expression Regulation, Bacterial, Genes, Bacterial, Membrane Transport Proteins/metabolism, Mutation, Protein Folding, Protein Transport/physiology, Stress, Physiological/physiology, Substrate Specificity