Gene amplifications cause high-level resistance against albicidin in gram-negative bacteria.

Antibiotic resistance is a continuously increasing concern for public healthcare. Understanding resistance mechanisms and their emergence is crucial for the development of new antibiotics and their effective use. The peptide antibiotic albicidin is such a promising candidate that, as a gyrase poison...

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Main Authors: Mareike Saathoff, Simone Kosol, Torsten Semmler, Karsten Tedin, Nicole Dimos, Johannes Kupke, Maria Seidel, Fereshteh Ghazisaeedi, Micela Condor Jonske, Silver A Wolf, Benno Kuropka, Wojciech Czyszczoń, Dmitry Ghilarov, Stefan Grätz, Jonathan G Heddle, Bernhard Loll, Roderich D Süssmuth, Marcus Fulde
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-08-01
Series:PLoS Biology
Online Access:https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3002186&type=printable
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author Mareike Saathoff
Simone Kosol
Torsten Semmler
Karsten Tedin
Nicole Dimos
Johannes Kupke
Maria Seidel
Fereshteh Ghazisaeedi
Micela Condor Jonske
Silver A Wolf
Benno Kuropka
Wojciech Czyszczoń
Dmitry Ghilarov
Stefan Grätz
Jonathan G Heddle
Bernhard Loll
Roderich D Süssmuth
Marcus Fulde
author_facet Mareike Saathoff
Simone Kosol
Torsten Semmler
Karsten Tedin
Nicole Dimos
Johannes Kupke
Maria Seidel
Fereshteh Ghazisaeedi
Micela Condor Jonske
Silver A Wolf
Benno Kuropka
Wojciech Czyszczoń
Dmitry Ghilarov
Stefan Grätz
Jonathan G Heddle
Bernhard Loll
Roderich D Süssmuth
Marcus Fulde
author_sort Mareike Saathoff
collection DOAJ
description Antibiotic resistance is a continuously increasing concern for public healthcare. Understanding resistance mechanisms and their emergence is crucial for the development of new antibiotics and their effective use. The peptide antibiotic albicidin is such a promising candidate that, as a gyrase poison, shows bactericidal activity against a wide range of gram-positive and gram-negative bacteria. Here, we report the discovery of a gene amplification-based mechanism that imparts an up to 1000-fold increase in resistance levels against albicidin. RNA sequencing and proteomics data show that this novel mechanism protects Salmonella Typhimurium and Escherichia coli by increasing the copy number of STM3175 (YgiV), a transcription regulator with a GyrI-like small molecule binding domain that traps albicidin with high affinity. X-ray crystallography and molecular docking reveal a new conserved motif in the binding groove of the GyrI-like domain that can interact with aromatic building blocks of albicidin. Phylogenetic studies suggest that this resistance mechanism is ubiquitous in gram-negative bacteria, and our experiments confirm that STM3175 homologs can confer resistance in pathogens such as Vibrio vulnificus and Pseudomonas aeruginosa.
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issn 1544-9173
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language English
publishDate 2023-08-01
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spelling doaj-art-eeba2ab4be8d437b83a1dd0386ce840c2025-08-20T03:01:22ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852023-08-01218e300218610.1371/journal.pbio.3002186Gene amplifications cause high-level resistance against albicidin in gram-negative bacteria.Mareike SaathoffSimone KosolTorsten SemmlerKarsten TedinNicole DimosJohannes KupkeMaria SeidelFereshteh GhazisaeediMicela Condor JonskeSilver A WolfBenno KuropkaWojciech CzyszczońDmitry GhilarovStefan GrätzJonathan G HeddleBernhard LollRoderich D SüssmuthMarcus FuldeAntibiotic resistance is a continuously increasing concern for public healthcare. Understanding resistance mechanisms and their emergence is crucial for the development of new antibiotics and their effective use. The peptide antibiotic albicidin is such a promising candidate that, as a gyrase poison, shows bactericidal activity against a wide range of gram-positive and gram-negative bacteria. Here, we report the discovery of a gene amplification-based mechanism that imparts an up to 1000-fold increase in resistance levels against albicidin. RNA sequencing and proteomics data show that this novel mechanism protects Salmonella Typhimurium and Escherichia coli by increasing the copy number of STM3175 (YgiV), a transcription regulator with a GyrI-like small molecule binding domain that traps albicidin with high affinity. X-ray crystallography and molecular docking reveal a new conserved motif in the binding groove of the GyrI-like domain that can interact with aromatic building blocks of albicidin. Phylogenetic studies suggest that this resistance mechanism is ubiquitous in gram-negative bacteria, and our experiments confirm that STM3175 homologs can confer resistance in pathogens such as Vibrio vulnificus and Pseudomonas aeruginosa.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3002186&type=printable
spellingShingle Mareike Saathoff
Simone Kosol
Torsten Semmler
Karsten Tedin
Nicole Dimos
Johannes Kupke
Maria Seidel
Fereshteh Ghazisaeedi
Micela Condor Jonske
Silver A Wolf
Benno Kuropka
Wojciech Czyszczoń
Dmitry Ghilarov
Stefan Grätz
Jonathan G Heddle
Bernhard Loll
Roderich D Süssmuth
Marcus Fulde
Gene amplifications cause high-level resistance against albicidin in gram-negative bacteria.
PLoS Biology
title Gene amplifications cause high-level resistance against albicidin in gram-negative bacteria.
title_full Gene amplifications cause high-level resistance against albicidin in gram-negative bacteria.
title_fullStr Gene amplifications cause high-level resistance against albicidin in gram-negative bacteria.
title_full_unstemmed Gene amplifications cause high-level resistance against albicidin in gram-negative bacteria.
title_short Gene amplifications cause high-level resistance against albicidin in gram-negative bacteria.
title_sort gene amplifications cause high level resistance against albicidin in gram negative bacteria
url https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3002186&type=printable
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