Associations between sensitivity to antibiotics, disinfectants and heavy metals in natural, clinical and laboratory isolates of <scp><i>Escherichia coli</i></scp>

Bischofberger, Anna M.; Baumgärtner, Michael; Pfrunder‐Cardozo, Katia R.; Allen, Richard C.; Hall, Alex R.

doi:10.1111/1462-2920.14986

Cited by 13 publications

(9 citation statements)

References 77 publications

(100 reference statements)

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“…Metals that exhibit antimicrobial properties are used as alternatives to antibiotics in farming and agriculture. Nevertheless, the use of metals at high concentrations contributes to environment contamination and to co‐selection of antibiotic resistance genes (Baker‐Austin et al , 2006; Purves et al , 2018; Rensing et al , 2018; Bischofberger et al , 2020). The combination of excess Cu 2+ , at very low concentration, and iron limitation poses a serious challenge to bacteria as shown in this work.…”

Section: Discussionmentioning

confidence: 99%

Increasing the copper sensitivity of microorganisms by restricting iron supply, a strategy for bio‐management practices

Steunou

Bourbon

Babot

et al. 2020

Microbial Biotechnology

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Pollution by copper (Cu 2+) extensively used as antimicrobial in agriculture and farming represents a threat to the environment and human health. Finding ways to make microorganisms sensitive to lower metal concentrations could help decreasing the use of Cu 2+ in agriculture. In this respect, we showed that limiting iron (Fe) uptake makes bacteria much more susceptible to Cu 2+ or Cd 2+ poisoning. Using efflux mutants of the purple bacterium Rubrivivax gelatinosus, we showed that Cu + and Cd 2+ resistance relies on the expression of the Fur-regulated FbpABC and Ftr iron transporters. To support this conclusion, inactivation of these Fe-importers in the Cu + or Cd 2+-ATPase efflux mutants gave rise to hypersensitivity towards these ions. Moreover, in metal overloaded cells the expression of FbpA, the periplasmic iron-binding component of the ferric ion transport FbpABC system was induced, suggesting that cells perceived an 'iron-starvation' situation and responded to it by inducing Fe-importers. In this context, the Fe-Sod activity increased in response to Fe homoeostasis dysregulation. Similar results were obtained for Vibrio cholerae and Escherichia coli, suggesting that perturbation of Fe homoeostasis by metal excess appeared as an adaptive response commonly used by a variety of bacteria. The presented data support a model in which metal excess induces Fe-uptake to support [4Fe-4S] synthesis and thereby induce ROS detoxification system.

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Section: Discussionmentioning

confidence: 99%

Increasing the copper sensitivity of microorganisms by restricting iron supply, a strategy for bio‐management practices

Steunou

Bourbon

Babot

et al. 2020

Microbial Biotechnology

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“…Other studies have associated a decrease in BKC susceptibility with a change in bacterial cytoplasmic membrane composition (Bisbiroulas et al, 2011;Bischofberger et al, 2020;Ceragioli et al, 2010;Guérin-Méchin et al, 2004;Jennings et al, 2017;Maertens et al, 2020;Noll et al, 2020;Voumard et al, 2020), outer membrane protein (Ishikawa et al, 2002;Pereira et al, 2021;Tabata et al, 2003) or outer membrane (Chen et al, 2014;Ishikawa et al, 2002;Joynson et al, 2002;Loughlin et al, 2002;Manniello et al, 1978;Nordholt et al, 2021). One study attributed a decrease in BKC susceptibility associated with an increase in MIC to some antibiotics to a combination of mutations and efflux (Kim et al, 2018).…”

Section: Other Mechanisms Involved In Decreased Bkc Susceptibilitymentioning

confidence: 99%

“…(Mavri & Smole Možina, 2013 ), A. baumannii (Khosravi et al, 2021 ; Srinivasan et al, 2009 ) and L. monocytogenes (Gray et al, 2021 ; Kremer et al, 2017 ). In six studies, both a change in efflux and membrane properties were associated with decreased susceptibility to BKC (Bischofberger et al, 2020 ; Fernández‐Cuenca et al, 2015 ; Langsrud et al, 2004 ; Mavri & Smole Možina, 2013 ; Nagai et al, 2003 ; Pereira et al, 2021 ). A few investigations looked at ad litteram ‘inducible resistance’ (as defined in this review inducible reduced susceptibility) when bacteria were exposed to BKC.…”

Section: Benzalkonium Chloride and Bacterial ‘Resistance’mentioning

confidence: 99%

Impact of benzalkonium chloride, benzethonium chloride and chloroxylenol on bacterial antimicrobial resistance

Maillard

2022

Journal of Applied Microbiology

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This review examined 3655 articles on benzalkonium chloride (BKC), benzethonium chloride (BZT) and chloroxylenol (CHO) aiming to understand their impact on antimicrobial resistance. Following the application of inclusion/exclusion criteria, only 230 articles were retained for analysis; 212 concerned BKC, with only 18 for CHO and BZT. Seventy-eight percent of studies used MIC to measure BKC efficacy. Very few studies defined the term 'resistance' and 85% of studies defined 'resistance' as <10fold increase (40% as low as 2-fold) in MIC. Only a few in vitro studies reported on formulated products and when they did, products performed better. In vitro studies looking at the impact of BKC exposure on bacterial resistance used either a stepwise training protocol or exposure to constant BKC concentrations. In these, BKC exposure resulted in elevated MIC or/and MBC, often associated with efflux, and at time, a change in antibiotic susceptibility profile. The clinical relevance of these findings was, however, neither reported nor addressed. Of note, several studies reported that bacterial strains with an elevated MIC or MBC remained susceptible to the in-use BKC concentration. BKC exposure was shown to reduce bacterial diversity in complex microbial microcosms, although the clinical significance of such a change has not been established. The impact of BKC exposure on the dissemination of resistant genes (notably efflux) remains speculative, although it manifests that clinical, veterinary and food isolates with elevated BKC MIC carried multiple efflux pump genes. The correlation between BKC usage and gene carriage, maintenance and dissemination has also not been established. The lack of clinical interpretation and significance in these studies does not allow to establish with certainty the role of BKC on AMR in practice. The limited literature and BZT and CHO do not allow to conclude that these will impact negatively on emerging bacterial resistance in practice.

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“…Copper and zinc exhibit antimicrobial properties and are used as alternatives to antibiotics in farming and agriculture. Nevertheless, the use of high concentrations of these cations led to environment contamination and to co‐selection of antibiotic resistance genes (Baker‐Austin et al , 2006; Purves et al ., 2018; Rensing et al , 2018; Bischofberger et al ., 2020). To avoid such impacts, we need to significantly reduce the concentration of metal in metal‐based antimicrobial treatments.…”

Section: Discussionmentioning

confidence: 99%

Additive effects of metal excess and superoxide, a highly toxic mixture in bacteria

Steunou

Babot

Bourbon

et al. 2020

Microbial Biotechnology

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Heavy metal contamination is a serious environmental problem. Understanding the toxicity mechanisms may allow to lower concentration of metals in the metal-based antimicrobial treatments of crops, and reduce metal content in soil and groundwater. Here, we investigate the interplay between metal efflux systems and the superoxide dismutase (SOD) in the purple bacterium Rubrivivax gelatinosus and other bacteria through analysis of the impact of metal accumulation. Exposure of the Cd 2+-efflux mutant DcadA to Cd 2+ caused an increase in the amount and activity of the cytosolic Fe-Sod SodB, thereby suggesting a role of SodB in the protection against Cd 2+. In support of this conclusion, inactivation of sodB gene in the DcadA cells alleviated detoxification of superoxide and enhanced Cd 2+ toxicity. Similar findings were described in the Cu +-efflux mutant with Cu +. Induction of the Mn-Sod or Fe-Sod in response to metals in other bacteria, including Escherichia coli, Pseudomonas aeruginosa, Pseudomonas putida, Vibrio cholera and Bacillus subtilis, was also shown. Both excess Cd 2+ or Cu + and superoxide can damage [4Fe-4S] clusters. The additive effect of metal and superoxide on the [4Fe-4S] could therefore explain the hypersensitive phenotype in mutants lacking SOD and the efflux ATPase. These findings underscore that ROS defence system becomes decisive for bacterial survival under metal excess.

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Associations between sensitivity to antibiotics, disinfectants and heavy metals in natural, clinical and laboratory isolates of Escherichia coli

Cited by 13 publications

References 77 publications

Increasing the copper sensitivity of microorganisms by restricting iron supply, a strategy for bio‐management practices

Increasing the copper sensitivity of microorganisms by restricting iron supply, a strategy for bio‐management practices

Impact of benzalkonium chloride, benzethonium chloride and chloroxylenol on bacterial antimicrobial resistance

Additive effects of metal excess and superoxide, a highly toxic mixture in bacteria

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