Multiple Compounds Secreted by <italic toggle="yes">Pseudomonas aeruginosa</italic> Increase the Tolerance of <italic toggle="yes">Staphylococcus aureus</italic> to the Antimicrobial Metals Copper and Silver

ABSTRACT Metal-based antimicrobials have been used for thousands of years to treat and prevent bacterial infections. Currently, both silver and copper are used in health care and industry to prevent and treat the spread of harmful bacteria. However, like most antimicrobial agents, their efficacy aga...

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Autores principales: Nadia K. Monych, Raymond J. Turner
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:d532f998672b4c4a849295820096c4a32021-12-02T19:47:33ZMultiple Compounds Secreted by <italic toggle="yes">Pseudomonas aeruginosa</italic> Increase the Tolerance of <italic toggle="yes">Staphylococcus aureus</italic> to the Antimicrobial Metals Copper and Silver10.1128/mSystems.00746-202379-5077https://doaj.org/article/d532f998672b4c4a849295820096c4a32020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00746-20https://doaj.org/toc/2379-5077ABSTRACT Metal-based antimicrobials have been used for thousands of years to treat and prevent bacterial infections. Currently, both silver and copper are used in health care and industry to prevent and treat the spread of harmful bacteria. However, like most antimicrobial agents, their efficacy against polymicrobial infections has not been fully elucidated. Coinfection with Pseudomonas aeruginosa and Staphylococcus aureus and the resulting interactions have been implicated in higher virulence, antibiotic resistance, and increased chronic infections. Here, the influence of secreted compounds from P. aeruginosa on metal antimicrobial tolerance in S. aureus was examined. This study determined that multiple compounds from P. aeruginosa increase the tolerance of S. aureus to copper and/or silver when cultured in simulated wound fluid. The presence of these secreted compounds from P. aeruginosa during exposure of S. aureus to copper or silver increased the MIC from 500 μM to 2,000 μM for copper and 16 to 63 μM for silver. The contribution of specific compounds to S. aureus tolerance was determined using gene deletion and disruption mutants, and metabolite analysis. Compounds identified as potential contributors were then individually added to S. aureus during metal exposure. Copper tolerance in S. aureus was found to be increased by amino acids and dihydroaeruginoate (Dha) secreted by P. aeruginosa. The silver tolerance provided to S. aureus was influenced only by two amino acids, serine and threonine, as well as the Pseudomonas quinolone signal (PQS) molecules from P. aeruginosa. IMPORTANCE Alternative antimicrobials, such as metals, are one of the methods currently used to help mitigate antibiotic resistance. Metal-based antimicrobials such as copper and silver are used currently both to prevent and to treat infections. Although the efficacy of these antimicrobials has been determined in single-species culture, bacteria rarely exist in a single-species group in the environment. Both Pseudomonas aeruginosa and Staphylococcus aureus are often found associated with each other in severe chronic infections displaying increased virulence and antibiotic tolerance. In this study, we determined that multiple compounds secreted by P. aeruginosa are able to increase the tolerance of S. aureus to both copper and silver. This work demonstrates the expansive chemical communication occurring in polymicrobial infections between bacteria.Nadia K. MonychRaymond J. TurnerAmerican Society for MicrobiologyarticlePseudomonas aeruginosaStaphylococcus aureusantimicrobialbacterial interactionscoppermetal resistanceMicrobiologyQR1-502ENmSystems, Vol 5, Iss 5 (2020)
institution DOAJ
collection DOAJ
language EN
topic Pseudomonas aeruginosa
Staphylococcus aureus
antimicrobial
bacterial interactions
copper
metal resistance
Microbiology
QR1-502
spellingShingle Pseudomonas aeruginosa
Staphylococcus aureus
antimicrobial
bacterial interactions
copper
metal resistance
Microbiology
QR1-502
Nadia K. Monych
Raymond J. Turner
Multiple Compounds Secreted by <italic toggle="yes">Pseudomonas aeruginosa</italic> Increase the Tolerance of <italic toggle="yes">Staphylococcus aureus</italic> to the Antimicrobial Metals Copper and Silver
description ABSTRACT Metal-based antimicrobials have been used for thousands of years to treat and prevent bacterial infections. Currently, both silver and copper are used in health care and industry to prevent and treat the spread of harmful bacteria. However, like most antimicrobial agents, their efficacy against polymicrobial infections has not been fully elucidated. Coinfection with Pseudomonas aeruginosa and Staphylococcus aureus and the resulting interactions have been implicated in higher virulence, antibiotic resistance, and increased chronic infections. Here, the influence of secreted compounds from P. aeruginosa on metal antimicrobial tolerance in S. aureus was examined. This study determined that multiple compounds from P. aeruginosa increase the tolerance of S. aureus to copper and/or silver when cultured in simulated wound fluid. The presence of these secreted compounds from P. aeruginosa during exposure of S. aureus to copper or silver increased the MIC from 500 μM to 2,000 μM for copper and 16 to 63 μM for silver. The contribution of specific compounds to S. aureus tolerance was determined using gene deletion and disruption mutants, and metabolite analysis. Compounds identified as potential contributors were then individually added to S. aureus during metal exposure. Copper tolerance in S. aureus was found to be increased by amino acids and dihydroaeruginoate (Dha) secreted by P. aeruginosa. The silver tolerance provided to S. aureus was influenced only by two amino acids, serine and threonine, as well as the Pseudomonas quinolone signal (PQS) molecules from P. aeruginosa. IMPORTANCE Alternative antimicrobials, such as metals, are one of the methods currently used to help mitigate antibiotic resistance. Metal-based antimicrobials such as copper and silver are used currently both to prevent and to treat infections. Although the efficacy of these antimicrobials has been determined in single-species culture, bacteria rarely exist in a single-species group in the environment. Both Pseudomonas aeruginosa and Staphylococcus aureus are often found associated with each other in severe chronic infections displaying increased virulence and antibiotic tolerance. In this study, we determined that multiple compounds secreted by P. aeruginosa are able to increase the tolerance of S. aureus to both copper and silver. This work demonstrates the expansive chemical communication occurring in polymicrobial infections between bacteria.
format article
author Nadia K. Monych
Raymond J. Turner
author_facet Nadia K. Monych
Raymond J. Turner
author_sort Nadia K. Monych
title Multiple Compounds Secreted by <italic toggle="yes">Pseudomonas aeruginosa</italic> Increase the Tolerance of <italic toggle="yes">Staphylococcus aureus</italic> to the Antimicrobial Metals Copper and Silver
title_short Multiple Compounds Secreted by <italic toggle="yes">Pseudomonas aeruginosa</italic> Increase the Tolerance of <italic toggle="yes">Staphylococcus aureus</italic> to the Antimicrobial Metals Copper and Silver
title_full Multiple Compounds Secreted by <italic toggle="yes">Pseudomonas aeruginosa</italic> Increase the Tolerance of <italic toggle="yes">Staphylococcus aureus</italic> to the Antimicrobial Metals Copper and Silver
title_fullStr Multiple Compounds Secreted by <italic toggle="yes">Pseudomonas aeruginosa</italic> Increase the Tolerance of <italic toggle="yes">Staphylococcus aureus</italic> to the Antimicrobial Metals Copper and Silver
title_full_unstemmed Multiple Compounds Secreted by <italic toggle="yes">Pseudomonas aeruginosa</italic> Increase the Tolerance of <italic toggle="yes">Staphylococcus aureus</italic> to the Antimicrobial Metals Copper and Silver
title_sort multiple compounds secreted by <italic toggle="yes">pseudomonas aeruginosa</italic> increase the tolerance of <italic toggle="yes">staphylococcus aureus</italic> to the antimicrobial metals copper and silver
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/d532f998672b4c4a849295820096c4a3
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