Protozoan predation enhances stress resistance and antibiotic tolerance in Burkholderia cenocepacia by triggering the SOS response

  1. Morón García, Álvaro 12
  2. Tarhouchi, Alaa E 12
  3. Belinchón Esteban, Iván 12
  4. Valenzuela, Juan M 12
  5. Francisco Martínez, Patricia de 12
  6. Martín González, Ana 12
  7. Amaro Torres, Francisco 12
  1. 1 Department of Genetics , Physiology and Microbiology. Faculty of Biological Sciences, Madrid 28040 , Spain
  2. 2 Complutense University of Madrid , Physiology and Microbiology. Faculty of Biological Sciences, Madrid 28040 , Spain
Revista:
The ISME Journal

ISSN: 1751-7362,  1751-7370

Año de publicación: 2024

Volumen: 18

Número: 1

Tipo: Artículo

DOI: 10.1093/ISMEJO/WRAE014 GOOGLE SCHOLAR lock_openAcceso abierto editor

Otras publicaciones en: The ISME Journal

Resumen

Bacterivorous protists are thought to serve as training grounds for bacterial pathogens by subjecting them to the same hostile conditions that they will encounter in the human host. Bacteria that survive intracellular digestion exhibit enhanced virulence and stress resistance after successful passage through protozoa but the underlying mechanisms are unknown. Here we show that the opportunistic pathogen Burkholderia cenocepacia survives phagocytosis by ciliates found in domestic and hospital sink drains, and viable bacteria are expelled packaged in respirable membrane vesicles with enhanced resistance to oxidative stress, desiccation, and antibiotics, thereby contributing to pathogen dissemination in the environment. Reactive oxygen species generated within the protozoan phagosome promote the formation of persisters tolerant to ciprofloxacin by activating the bacterial SOS response. In addition, we show that genes encoding antioxidant enzymes are upregulated during passage through ciliates increasing bacterial resistance to oxidative radicals. We prove that suppression of the SOS response impairs bacterial intracellular survival and persister formation within protists. This study highlights the significance of protozoan food vacuoles as niches that foster bacterial adaptation in natural and built environments and suggests that persister switch within phagosomes may be a widespread phenomenon in bacteria surviving intracellular digestion.

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