Biofilm antimicrobial susceptibility through an experimental evolutionary lens

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Abstract

Experimental evolution experiments in which bacterial populations are repeatedly exposed to an antimicrobial treatment, and examination of the genotype and phenotype of the resulting evolved bacteria, can help shed light on mechanisms behind reduced susceptibility. In this review we present an overview of why it is important to include biofilms in experimental evolution, which approaches are available to study experimental evolution in biofilms and what experimental evolution has taught us about tolerance and resistance in biofilms. Finally, we present an emerging consensus view on biofilm antimicrobial susceptibility supported by data obtained during experimental evolution studies.

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A common mechanism of cellular death induced by bactericidal antibiotics.

Michael A Kohanski, Daniel Dwyer, Boris Hayete … (2007)

Antibiotic mode-of-action classification is based upon drug-target interaction and whether the resultant inhibition of cellular function is lethal to bacteria. Here we show that the three major classes of bactericidal antibiotics, regardless of drug-target interaction, stimulate the production of highly deleterious hydroxyl radicals in Gram-negative and Gram-positive bacteria, which ultimately contribute to cell death. We also show, in contrast, that bacteriostatic drugs do not produce hydroxyl radicals. We demonstrate that the mechanism of hydroxyl radical formation induced by bactericidal antibiotics is the end product of an oxidative damage cellular death pathway involving the tricarboxylic acid cycle, a transient depletion of NADH, destabilization of iron-sulfur clusters, and stimulation of the Fenton reaction. Our results suggest that all three major classes of bactericidal drugs can be potentiated by targeting bacterial systems that remediate hydroxyl radical damage, including proteins involved in triggering the DNA damage response, e.g., RecA.

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Physiological heterogeneity in biofilms.

Philip Stewart, Michael J Franklin (2008)

Biofilms contain bacterial cells that are in a wide range of physiological states. Within a biofilm population, cells with diverse genotypes and phenotypes that express distinct metabolic pathways, stress responses and other specific biological activities are juxtaposed. The mechanisms that contribute to this genetic and physiological heterogeneity include microscale chemical gradients, adaptation to local environmental conditions, stochastic gene expression and the genotypic variation that occurs through mutation and selection. Here, we discuss the processes that generate chemical gradients in biofilms, the genetic and physiological responses of the bacteria as they adapt to these gradients and the techniques that can be used to visualize and measure the microscale physiological heterogeneities of bacteria in biofilms.

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Bacterial competition: surviving and thriving in the microbial jungle.

Michael Hibbing, Clay Fuqua, Matthew Parsek … (2010)

Most natural environments harbour a stunningly diverse collection of microbial species. In these communities, bacteria compete with their neighbours for space and resources. Laboratory experiments with pure and mixed cultures have revealed many active mechanisms by which bacteria can impair or kill other microorganisms. In addition, a growing body of theoretical and experimental population studies indicates that the interactions within and between bacterial species can have a profound impact on the outcome of competition in nature. The next challenge is to integrate the findings of these laboratory and theoretical studies and to evaluate the predictions that they generate in more natural settings.

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Author and article information

Contributors

Tom Coenye:

ORCID: http://orcid.org/0000-0002-6407-0601

Tom.Coenye@UGent.be

Journal

Journal ID (nlm-ta): NPJ Biofilms Microbiomes

Journal ID (iso-abbrev): NPJ Biofilms Microbiomes

Title: NPJ Biofilms and Microbiomes

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2055-5008

Publication date (Electronic): 18 October 2022

Publication date PMC-release: 18 October 2022

Publication date Collection: 2022

Volume: 8

Electronic Location Identifier: 82

Affiliations

[1 ]GRID grid.5342.0, ISNI 0000 0001 2069 7798, Laboratory of Pharmaceutical Microbiology, , Ghent University, ; Ghent, Belgium

[2 ]GRID grid.5254.6, ISNI 0000 0001 0674 042X, Costerton Biofilm Center, , University of Copenhagen, ; Copenhagen, Denmark

Author information

Tom Coenye http://orcid.org/0000-0002-6407-0601

Thomas Bjarnsholt http://orcid.org/0000-0002-8003-7414

Article

Publisher ID: 346

DOI: 10.1038/s41522-022-00346-4

PMC ID: 9579162

PubMed ID: 36257971

SO-VID: 6be82a20-390c-4054-b4f7-3ea649a4cb36

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 7 June 2022

Date accepted : 4 October 2022

Funding

Funded by: FundRef https://doi.org/10.13039/501100003554, Lundbeckfonden (Lundbeck Foundation);

Award ID: R364-2021-1474

Award Recipient : Tom Coenye Thomas Bjarnsholt

Funded by: FundRef https://doi.org/10.13039/501100003130, Fonds Wetenschappelijk Onderzoek (Research Foundation Flanders);

Award ID: V401322N

Award Recipient : Tom Coenye

Funded by: FundRef https://doi.org/10.13039/501100007229, Bijzonder Onderzoeksfonds (Special Research Fund);

Award ID: BOF.DOC.2018.0023.01

Award Recipient : Mona Bové

Custom metadata

Keywords: biofilms,molecular evolution,antimicrobials

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Keywords: biofilms, molecular evolution, antimicrobials

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Biofilm antimicrobial susceptibility through an experimental evolutionary lens

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Abstract

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Most cited references 111

A common mechanism of cellular death induced by bactericidal antibiotics.

Physiological heterogeneity in biofilms.

Bacterial competition: surviving and thriving in the microbial jungle.

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Cited by 15

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