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

Summary Pollution by copper (Cu2+) 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 Cu2+ in agriculture. In this respect,...

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Main Authors: Anne Soisig Steunou, Marie‐Line Bourbon, Marion Babot, Anne Durand, Sylviane Liotenberg, Yoshiharu Yamaichi, Soufian Ouchane
Format: Article
Language:English
Published: Wiley 2020-09-01
Series:Microbial Biotechnology
Online Access:https://doi.org/10.1111/1751-7915.13590
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spelling doaj-5bea958c20994b3a80d106e625b634cb2020-11-25T02:54:21ZengWileyMicrobial Biotechnology1751-79152020-09-011351530154510.1111/1751-7915.13590Increasing the copper sensitivity of microorganisms by restricting iron supply, a strategy for bio‐management practicesAnne Soisig Steunou0Marie‐Line Bourbon1Marion Babot2Anne Durand3Sylviane Liotenberg4Yoshiharu Yamaichi5Soufian Ouchane6Institute for Integrative Biology of the Cell (I2BC) CEA CNRS Université Paris‐Saclay 91198 Gif‐sur‐Yvette FranceInstitute for Integrative Biology of the Cell (I2BC) CEA CNRS Université Paris‐Saclay 91198 Gif‐sur‐Yvette FranceInstitute for Integrative Biology of the Cell (I2BC) CEA CNRS Université Paris‐Saclay 91198 Gif‐sur‐Yvette FranceInstitute for Integrative Biology of the Cell (I2BC) CEA CNRS Université Paris‐Saclay 91198 Gif‐sur‐Yvette FranceInstitute for Integrative Biology of the Cell (I2BC) CEA CNRS Université Paris‐Saclay 91198 Gif‐sur‐Yvette FranceInstitute for Integrative Biology of the Cell (I2BC) CEA CNRS Université Paris‐Saclay 91198 Gif‐sur‐Yvette FranceInstitute for Integrative Biology of the Cell (I2BC) CEA CNRS Université Paris‐Saclay 91198 Gif‐sur‐Yvette FranceSummary Pollution by copper (Cu2+) 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 Cu2+ in agriculture. In this respect, we showed that limiting iron (Fe) uptake makes bacteria much more susceptible to Cu2+ or Cd2+ poisoning. Using efflux mutants of the purple bacterium Rubrivivax gelatinosus, we showed that Cu+ and Cd2+ 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 Cd2+‐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.https://doi.org/10.1111/1751-7915.13590
collection DOAJ
language English
format Article
sources DOAJ
author Anne Soisig Steunou
Marie‐Line Bourbon
Marion Babot
Anne Durand
Sylviane Liotenberg
Yoshiharu Yamaichi
Soufian Ouchane
spellingShingle Anne Soisig Steunou
Marie‐Line Bourbon
Marion Babot
Anne Durand
Sylviane Liotenberg
Yoshiharu Yamaichi
Soufian Ouchane
Increasing the copper sensitivity of microorganisms by restricting iron supply, a strategy for bio‐management practices
Microbial Biotechnology
author_facet Anne Soisig Steunou
Marie‐Line Bourbon
Marion Babot
Anne Durand
Sylviane Liotenberg
Yoshiharu Yamaichi
Soufian Ouchane
author_sort Anne Soisig Steunou
title Increasing the copper sensitivity of microorganisms by restricting iron supply, a strategy for bio‐management practices
title_short Increasing the copper sensitivity of microorganisms by restricting iron supply, a strategy for bio‐management practices
title_full Increasing the copper sensitivity of microorganisms by restricting iron supply, a strategy for bio‐management practices
title_fullStr Increasing the copper sensitivity of microorganisms by restricting iron supply, a strategy for bio‐management practices
title_full_unstemmed Increasing the copper sensitivity of microorganisms by restricting iron supply, a strategy for bio‐management practices
title_sort increasing the copper sensitivity of microorganisms by restricting iron supply, a strategy for bio‐management practices
publisher Wiley
series Microbial Biotechnology
issn 1751-7915
publishDate 2020-09-01
description Summary Pollution by copper (Cu2+) 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 Cu2+ in agriculture. In this respect, we showed that limiting iron (Fe) uptake makes bacteria much more susceptible to Cu2+ or Cd2+ poisoning. Using efflux mutants of the purple bacterium Rubrivivax gelatinosus, we showed that Cu+ and Cd2+ 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 Cd2+‐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.
url https://doi.org/10.1111/1751-7915.13590
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