Extracellular vesicles as an alternative copper-secretion mechanism in bacteria

Metal homeostasis is fundamental for optimal performance of cell metabolic pathways. Over the course of evolution, several systems emerged to warrant an intracellular metal equilibrium. When exposed to growth-challenging copper concentrations, Gram-negative bacteria quickly activate copper-detoxific...

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Bibliographic Details
Authors: Lima, Steeve; Matinha-Cardoso, Jorge; Giner Lamia, Joaquín; Couto, Narciso; Pacheco, Catarina C.; Florencio Bellido, Francisco Javier; Wright, Phillip C.; Tamagnini, Paula; Oliveira, Paulo
Format: Article
Status:Published version
Publication date:2022
Country:España
Institution:Universidad de Sevilla (US)
Repository:idUS. Depósito de Investigación de la Universidad de Sevilla
OAI Identifier:oai:idus.us.es:11441/141879
Online Access:https://hdl.handle.net/11441/141879
https://doi.org/10.1016/j.jhazmat.2022.128594
Access Level:Open access
Keyword:Bacterial extracellular vesicles
Copper detoxification mechanisms
Copper secretion
Cyanobacteria
Metal homeostasis
Description
Summary:Metal homeostasis is fundamental for optimal performance of cell metabolic pathways. Over the course of evolution, several systems emerged to warrant an intracellular metal equilibrium. When exposed to growth-challenging copper concentrations, Gram-negative bacteria quickly activate copper-detoxification mechanisms, dependent on transmembrane-protein complexes and metallochaperones that mediate metal efflux. Here, we show that vesiculation is also a common bacterial response mechanism to high copper concentrations, and that extracellular vesicles (EVs) play a role in transporting copper. We present evidence that bacteria from different ecological niches release copious amounts of EVs when exposed to copper. Along with the activation of the classical detoxification systems, we demonstrate that copper-stressed cells of the cyanobacterium Synechocystis sp. PCC6803 release EVs loaded with the copper-binding metallochaperone CopM. Under standard growth conditions, CopM-loaded EVs could also be isolated from a Synechocystis strain lacking a functional TolC-protein, which we characterize here as exhibiting a copper-sensitive phenotype. Analyses of Synechocystis tolC-mutant's EVs isolated from cells cultivated under standard conditions indicated the presence of copper therein, in significantly higher levels as compared to those from the wild-type. Altogether, these results suggest that release of EVs in bacteria represent a novel copper-secretion mechanism, shedding light into alternative mechanisms of bacterial metal resistance.