Osmotic stress and vesiculation as key mechanisms controlling bacterial sensitivity and resistance to TiO2 nanoparticles

Commun Biol. 2021 Jun 3;4(1):678. doi: 10.1038/s42003-021-02213-y.

Abstract

Toxicity mechanisms of metal oxide nanoparticles towards bacteria and underlying roles of membrane composition are still debated. Herein, the response of lipopolysaccharide-truncated Escherichia coli K12 mutants to TiO2 nanoparticles (TiO2NPs, exposure in dark) is addressed at the molecular, single cell, and population levels by transcriptomics, fluorescence assays, cell nanomechanics and electrohydrodynamics. We show that outer core-free lipopolysaccharides featuring intact inner core increase cell sensitivity to TiO2NPs. TiO2NPs operate as membrane strippers, which induce osmotic stress, inactivate cell osmoregulation and initiate lipid peroxidation, which ultimately leads to genesis of membrane vesicles. In itself, truncation of lipopolysaccharide inner core triggers membrane permeabilization/depolarization, lipid peroxidation and hypervesiculation. In turn, it favors the regulation of TiO2NP-mediated changes in cell Turgor stress and leads to efficient vesicle-facilitated release of damaged membrane components. Remarkably, vesicles further act as electrostatic baits for TiO2NPs, thereby mitigating TiO2NPs toxicity. Altogether, we highlight antagonistic lipopolysaccharide-dependent bacterial responses to nanoparticles and we show that the destabilized membrane can generate unexpected resistance phenotype.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cytoplasmic Vesicles / drug effects*
  • Cytoplasmic Vesicles / metabolism
  • Drug Resistance, Bacterial / genetics
  • Escherichia coli / drug effects*
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism
  • Gene Expression Profiling / methods
  • Gene Expression Regulation, Bacterial / drug effects
  • Glucosyltransferases / genetics
  • Glucosyltransferases / metabolism
  • Glycosyltransferases / genetics
  • Glycosyltransferases / metabolism
  • Metal Nanoparticles / toxicity*
  • Microscopy, Atomic Force / methods
  • Mutation
  • Osmotic Pressure / drug effects*
  • Titanium / toxicity*

Substances

  • Escherichia coli Proteins
  • titanium dioxide
  • Titanium
  • Glycosyltransferases
  • Glucosyltransferases
  • WaaG protein, E coli
  • lipooligosaccharide 1,5-heptosyltransferase