Chromosomal Sil system contributes to silver resistance in E. coli ATCC 8739

Blanco Massani, Mariana; Klumpp, Jochen; Widmer, Madeleine; Speck, Christian; Nisple, Marc; Lehmann, Rainer; Schuppler, Markus

doi:10.1007/s10534-018-0143-1

Published: 04 October 2018

Chromosomal Sil system contributes to silver resistance in E. coli ATCC 8739

Mariana Blanco Massani ORCID: orcid.org/0000-0002-5053-6378^1,2,
Jochen Klumpp²,
Madeleine Widmer²,
Christian Speck²,
Marc Nisple²,
Rainer Lehmann²^nAff3 &
Markus Schuppler²

BioMetals volume 31, pages 1101–1114 (2018)Cite this article

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Abstract

The rise of antibiotic resistance in pathogenic bacteria is endangering the efficacy of antibiotics, which consequently results in greater use of silver as a biocide. Chromosomal mapping of the Cus system or plasmid encoded Sil system and their relationship with silver resistance was studied for several gram-negative bacteria. However, only few reports investigated silver detoxification mediated by the Sil system integrated in Escherichia coli chromosome. Accordingly, this work aimed to study the Sil system in E. coli ATCC 8739 and to produce evidence for its role in silver resistance development. Silver resistance was induced in E. coli ATCC 8739 by stepwise passage in culture media containing increasing concentrations of AgNO₃. The published genome of E. coli ATCC 8739 contains a region showing strong homology to the Sil system genes. The role of this region in E. coli ATCC 8739 was assessed by monitoring the expression of silC upon silver stress, which resulted in a 350-fold increased expression. De novo sequencing of the whole genome of a silver resistant strain derived from E. coli ATCC 8739 revealed mutations in ORFs putative for SilR and CusR. The silver resistant strain (E. coli AgNO₃R) showed constitutive expression of silC which posed a cost of fitness resulting in retarded growth. Furthermore, E. coli AgNO₃R exhibited cross-resistance to ciprofloxacin and a slightly increased tolerance to ampicillin. This study demonstrates that E. coli is able to develop resistance to silver, which may pose a threat towards an effective use of silver compounds as antiseptics.

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Acknowledgements

The authors are grateful for the support of MINCyT-ANPCyT, PICT Start-Up-2015-0027, PICT-2014-0585 and the National Institute of Industrial Technology (Argentina). The input given by Dr. Mario Hupfeld, Dr. Samuel Kilcher, and Dr. Matthew Dunne during the development of this work is also acknowledged.

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Rainer Lehmann
Present address: HeiQ Materials AG, Ruetistrasse 12, 8952 Schlieren, Zurich, Switzerland

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Instituto Nacional de Tecnología Industrial (INTI), Av. Gral. Paz 5445 (1650), San Martín, Argentina
Mariana Blanco Massani
Institute of Food, Nutrition and Health, ETH Zurich, Schmelzbergstrasse 7, 8092, Zurich, Switzerland
Mariana Blanco Massani, Jochen Klumpp, Madeleine Widmer, Christian Speck, Marc Nisple, Rainer Lehmann & Markus Schuppler

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Mariana Blanco Massani
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Jochen Klumpp
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Madeleine Widmer
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Christian Speck
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Marc Nisple
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Rainer Lehmann
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Markus Schuppler
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Correspondence to Mariana Blanco Massani.

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Blanco Massani, M., Klumpp, J., Widmer, M. et al. Chromosomal Sil system contributes to silver resistance in E. coli ATCC 8739. Biometals 31, 1101–1114 (2018). https://doi.org/10.1007/s10534-018-0143-1

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Received: 10 April 2018
Accepted: 25 September 2018
Published: 04 October 2018
Issue Date: December 2018
DOI: https://doi.org/10.1007/s10534-018-0143-1

Keywords

Silver resistance
Escherichia coli
De novo sequencing
Sil system
silC expression
qRT-PCR