Multiple genetic paths including massive gene amplification allow Mycobacterium tuberculosis to overcome loss of ESX-3 secretion system substrates

Proc Natl Acad Sci U S A. 2022 Feb 22;119(8):e2112608119. doi: 10.1073/pnas.2112608119.

Abstract

Mycobacterium tuberculosis (Mtb) possesses five type VII secretion systems (T7SS), virulence determinants that include the secretion apparatus and associated secretion substrates. Mtb strains deleted for the genes encoding substrates of the ESX-3 T7SS, esxG or esxH, require iron supplementation for in vitro growth and are highly attenuated in vivo. In a subset of infected mice, suppressor mutants of esxG or esxH deletions were isolated, which enabled growth to high titers or restored virulence. Suppression was conferred by mechanisms that cause overexpression of an ESX-3 paralogous region that lacks genes for the secretion apparatus but encodes EsxR and EsxS, apparent ESX-3 orphan substrates that functionally compensate for the lack of EsxG or EsxH. The mechanisms include the disruption of a transcriptional repressor and a massive 38- to 60-fold gene amplification. These data identify an iron acquisition regulon, provide insight into T7SS, and reveal a mechanism of Mtb chromosome evolution involving "accordion-type" amplification.

Keywords: ESX-3; Mycobacterium tuberculosis; TetR-family transcriptional regulator; genetic accordion; type VII secretion system.

MeSH terms

  • Animals
  • Bacterial Secretion Systems / genetics
  • Biological Evolution
  • Evolution, Molecular
  • Gene Amplification / genetics
  • Mice
  • Mycobacterium tuberculosis / genetics*
  • Mycobacterium tuberculosis / metabolism
  • Type VII Secretion Systems / genetics*
  • Type VII Secretion Systems / physiology
  • Virulence
  • Virulence Factors / genetics

Substances

  • Bacterial Secretion Systems
  • Type VII Secretion Systems
  • Virulence Factors