Regulation of major bacterial survival strategies by transcripts sequestration in a membraneless organelle

Tamar Szoke, Omer Goldberger, Nitsan Albocher-Kedem, Meshi Barsheshet, Nili Dezorella, Anat Nussbaum-Shochat, Reuven Wiener, Maya Schuldiner, Orna Amster-Choder*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

TmaR, the only known pole-localizer protein in Escherichia coli, was shown to cluster at the cell poles and control localization and activity of the major sugar regulator in a tyrosine phosphorylation-dependent manner. Here, we show that TmaR assembles by phase separation (PS) via heterotypic interactions with RNA in vivo and in vitro. An unbiased automated mutant screen combined with directed mutagenesis and genetic manipulations uncovered the importance of a predicted nucleic-acid-binding domain, a disordered region, and charged patches, one containing the phosphorylated tyrosine, for TmaR condensation. We demonstrate that, by protecting flagella-related transcripts, TmaR controls flagella production and, thus, cell motility and biofilm formation. These results connect PS in bacteria to survival and provide an explanation for the linkage between metabolism and motility. Intriguingly, a point mutation or increase in its cellular concentration induces irreversible liquid-to-solid transition of TmaR, similar to human disease-causing proteins, which affects cell morphology and division.

Original languageAmerican English
Article number113393
JournalCell Reports
Volume42
Issue number11
DOIs
StatePublished - 28 Nov 2023

Bibliographical note

Publisher Copyright:
© 2023 The Author(s)

Keywords

  • CP: Microbiology
  • PS
  • TmaR
  • aberrant condensates
  • bacterial cell organization
  • bacterial cell poles
  • bacterial motility
  • biomolecular condensates
  • control of flagella production
  • liquid-to-solid transition
  • phase separation

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