Characterizing the Mechanism of Action of an Ancient Antimicrobial, Manuka Honey, against <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Using Modern Transcriptomics

ABSTRACT Manuka honey has broad-spectrum antimicrobial activity, and unlike traditional antibiotics, resistance to its killing effects has not been reported. However, its mechanism of action remains unclear. Here, we investigated the mechanism of action of manuka honey and its key antibacterial comp...

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Autores principales:	Daniel Bouzo, Nural N. Cokcetin, Liping Li, Giulia Ballerin, Amy L. Bottomley, James Lazenby, Cynthia B. Whitchurch, Ian T. Paulsen, Karl A. Hassan, Elizabeth J. Harry
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Pseudomonas aeruginosa RNA-Seq antimicrobial activity honey manuka honey mechanism of action Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f6ebd7b8a8d8429f83a8e660cac184cf
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spelling	oai:doaj.org-article:f6ebd7b8a8d8429f83a8e660cac184cf2021-12-02T19:47:38ZCharacterizing the Mechanism of Action of an Ancient Antimicrobial, Manuka Honey, against <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Using Modern Transcriptomics10.1128/mSystems.00106-202379-5077https://doaj.org/article/f6ebd7b8a8d8429f83a8e660cac184cf2020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00106-20https://doaj.org/toc/2379-5077ABSTRACT Manuka honey has broad-spectrum antimicrobial activity, and unlike traditional antibiotics, resistance to its killing effects has not been reported. However, its mechanism of action remains unclear. Here, we investigated the mechanism of action of manuka honey and its key antibacterial components using a transcriptomic approach in a model organism, Pseudomonas aeruginosa. We show that no single component of honey can account for its total antimicrobial action, and that honey affects the expression of genes in the SOS response, oxidative damage, and quorum sensing. Manuka honey uniquely affects genes involved in the explosive cell lysis process and in maintaining the electron transport chain, causing protons to leak across membranes and collapsing the proton motive force, and it induces membrane depolarization and permeabilization in P. aeruginosa. These data indicate that the activity of manuka honey comes from multiple mechanisms of action that do not engender bacterial resistance. IMPORTANCE The threat of antimicrobial resistance to human health has prompted interest in complex, natural products with antimicrobial activity. Honey has been an effective topical wound treatment throughout history, predominantly due to its broad-spectrum antimicrobial activity. Unlike traditional antibiotics, honey-resistant bacteria have not been reported; however, honey remains underutilized in the clinic in part due to a lack of understanding of its mechanism of action. Here, we demonstrate that honey affects multiple processes in bacteria, and this is not explained by its major antibacterial components. Honey also uniquely affects bacterial membranes, and this can be exploited for combination therapy with antibiotics that are otherwise ineffective on their own. We argue that honey should be included as part of the current array of wound treatments due to its effective antibacterial activity that does not promote resistance in bacteria.Daniel BouzoNural N. CokcetinLiping LiGiulia BallerinAmy L. BottomleyJames LazenbyCynthia B. WhitchurchIan T. PaulsenKarl A. HassanElizabeth J. HarryAmerican Society for MicrobiologyarticlePseudomonas aeruginosaRNA-Seqantimicrobial activityhoneymanuka honeymechanism of actionMicrobiologyQR1-502ENmSystems, Vol 5, Iss 3 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Pseudomonas aeruginosa RNA-Seq antimicrobial activity honey manuka honey mechanism of action Microbiology QR1-502
spellingShingle	Pseudomonas aeruginosa RNA-Seq antimicrobial activity honey manuka honey mechanism of action Microbiology QR1-502 Daniel Bouzo Nural N. Cokcetin Liping Li Giulia Ballerin Amy L. Bottomley James Lazenby Cynthia B. Whitchurch Ian T. Paulsen Karl A. Hassan Elizabeth J. Harry Characterizing the Mechanism of Action of an Ancient Antimicrobial, Manuka Honey, against <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Using Modern Transcriptomics
description	ABSTRACT Manuka honey has broad-spectrum antimicrobial activity, and unlike traditional antibiotics, resistance to its killing effects has not been reported. However, its mechanism of action remains unclear. Here, we investigated the mechanism of action of manuka honey and its key antibacterial components using a transcriptomic approach in a model organism, Pseudomonas aeruginosa. We show that no single component of honey can account for its total antimicrobial action, and that honey affects the expression of genes in the SOS response, oxidative damage, and quorum sensing. Manuka honey uniquely affects genes involved in the explosive cell lysis process and in maintaining the electron transport chain, causing protons to leak across membranes and collapsing the proton motive force, and it induces membrane depolarization and permeabilization in P. aeruginosa. These data indicate that the activity of manuka honey comes from multiple mechanisms of action that do not engender bacterial resistance. IMPORTANCE The threat of antimicrobial resistance to human health has prompted interest in complex, natural products with antimicrobial activity. Honey has been an effective topical wound treatment throughout history, predominantly due to its broad-spectrum antimicrobial activity. Unlike traditional antibiotics, honey-resistant bacteria have not been reported; however, honey remains underutilized in the clinic in part due to a lack of understanding of its mechanism of action. Here, we demonstrate that honey affects multiple processes in bacteria, and this is not explained by its major antibacterial components. Honey also uniquely affects bacterial membranes, and this can be exploited for combination therapy with antibiotics that are otherwise ineffective on their own. We argue that honey should be included as part of the current array of wound treatments due to its effective antibacterial activity that does not promote resistance in bacteria.
format	article
author	Daniel Bouzo Nural N. Cokcetin Liping Li Giulia Ballerin Amy L. Bottomley James Lazenby Cynthia B. Whitchurch Ian T. Paulsen Karl A. Hassan Elizabeth J. Harry
author_facet	Daniel Bouzo Nural N. Cokcetin Liping Li Giulia Ballerin Amy L. Bottomley James Lazenby Cynthia B. Whitchurch Ian T. Paulsen Karl A. Hassan Elizabeth J. Harry
author_sort	Daniel Bouzo
title	Characterizing the Mechanism of Action of an Ancient Antimicrobial, Manuka Honey, against <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Using Modern Transcriptomics
title_short	Characterizing the Mechanism of Action of an Ancient Antimicrobial, Manuka Honey, against <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Using Modern Transcriptomics
title_full	Characterizing the Mechanism of Action of an Ancient Antimicrobial, Manuka Honey, against <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Using Modern Transcriptomics
title_fullStr	Characterizing the Mechanism of Action of an Ancient Antimicrobial, Manuka Honey, against <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Using Modern Transcriptomics
title_full_unstemmed	Characterizing the Mechanism of Action of an Ancient Antimicrobial, Manuka Honey, against <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Using Modern Transcriptomics
title_sort	characterizing the mechanism of action of an ancient antimicrobial, manuka honey, against <named-content content-type="genus-species">pseudomonas aeruginosa</named-content> using modern transcriptomics
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/f6ebd7b8a8d8429f83a8e660cac184cf
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Characterizing the Mechanism of Action of an Ancient Antimicrobial, Manuka Honey, against <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Using Modern Transcriptomics

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