Bacteroides expand the functional versatility of a conserved transcription factor and transcribed DNA to program capsule diversity

Nat Commun. 2024 Dec 30;15(1):10862. doi: 10.1038/s41467-024-55215-9.

Abstract

The genomes of human gut bacteria in the genus Bacteroides include numerous operons for biosynthesis of diverse capsular polysaccharides (CPSs). The first two genes of each CPS operon encode a locus-specific paralog of transcription elongation factor NusG (called UpxY), which enhances transcript elongation, and a UpxZ protein that inhibits noncognate UpxYs. This process, together with promoter inversions, ensures that a single CPS operon is transcribed in most cells. Here, we use in-vivo nascent-RNA sequencing and promoter-less in-vitro transcription (PIVoT) to show that UpxY recognizes a paused RNA polymerase via sequences in both the exposed non-template DNA and the upstream duplex DNA. UpxY association is aided by 'pause-then-escape' nascent RNA hairpins. UpxZ binds non-cognate UpxYs to directly inhibit UpxY association. This UpxY-UpxZ hierarchical regulatory program allows Bacteroides to generate subpopulations of cells producing diverse CPSs for optimal fitness.

MeSH terms

  • Bacterial Capsules* / genetics
  • Bacterial Capsules* / metabolism
  • Bacterial Proteins* / genetics
  • Bacterial Proteins* / metabolism
  • Bacteroides* / genetics
  • Bacteroides* / metabolism
  • DNA, Bacterial / genetics
  • DNA, Bacterial / metabolism
  • DNA-Directed RNA Polymerases / genetics
  • DNA-Directed RNA Polymerases / metabolism
  • Gene Expression Regulation, Bacterial*
  • Humans
  • Operon* / genetics
  • Promoter Regions, Genetic
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism
  • Transcription, Genetic*

Substances

  • Bacterial Proteins
  • Transcription Factors
  • DNA, Bacterial
  • DNA-Directed RNA Polymerases