A human pathogenic bacterium Shigella proliferates in plants through adoption of type III effectors for shigellosis

Plant Cell Environ. 2019 Nov;42(11):2962-2978. doi: 10.1111/pce.13603. Epub 2019 Jul 26.

Abstract

Shigella, which infects primates, can be transmitted via fresh vegetables; however, its molecular interactions with plants have not been elucidated. Here, we show that four Shigella strains, Shigella boydii, Shigella sonnei, Shigella flexneri 2a, and S. flexneri 5a, proliferate at different levels in Arabidopsis thaliana. Microscopic studies revealed that these bacteria were present inside leaves and damaged plant cells. Green fluorescent protein (GFP)-tagged S. boydii and S. flexneri 5a colonized leaves only, whereas S. flexneri 2a colonized both leaves and roots. Using Shigella mutants lacking type III secretion systems (T3SSs), we found that T3SSs that regulate the pathogenesis of shigellosis in humans also play a central role in bacterial proliferation in Arabidopsis. Strikingly, the immunosuppressive activity of two T3S effectors, OspF and OspG, was required for proliferation of Shigella in Arabidopsis. Of note, delivery of OspF or OspG effectors inside plant cells upon Shigella inoculation was confirmed using a split GFP system. These findings demonstrate that the human pathogen Shigella can proliferate in plants by adapting immunosuppressive machinery used in the original host human.

Keywords: Arabidopsis plants; PAMP-triggered immunity; Shigella spp.; T3S effectors; alternative host; enteropathogenic bacteria; proliferation; split GFP; trans-kingdom pathogenesis; type III secretion system (T3SS).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / immunology
  • Arabidopsis / metabolism
  • Arabidopsis / microbiology*
  • Bacterial Outer Membrane Proteins / metabolism*
  • Gene Expression Regulation, Plant / immunology
  • Plant Cells / microbiology
  • Plant Diseases / genetics
  • Plant Diseases / immunology
  • Plant Diseases / microbiology
  • Plant Leaves / microbiology
  • Plants, Genetically Modified
  • Shigella / genetics
  • Shigella / growth & development*
  • Shigella / pathogenicity*
  • Signal Transduction / immunology
  • Type III Secretion Systems / genetics
  • Type III Secretion Systems / metabolism*
  • Virulence Factors / metabolism*

Substances

  • Bacterial Outer Membrane Proteins
  • Type III Secretion Systems
  • Virulence Factors