Inhibition of multidrug-resistant foodborne Staphylococcus aureus biofilms by a natural terpenoid (+)-nootkatone and related molecular mechanism

Arakkaveettil Kabeer Farha; Qiong Qiong Yang; Gowoon Kim; Dan Zhang; Vuyo Mavumengwana; Olivier Habimana; Hua Bin Li; Harold Corke; Ren You Gan

doi:10.1016/j.foodcont.2020.107154

Inhibition of multidrug-resistant foodborne Staphylococcus aureus biofilms by a natural terpenoid (+)-nootkatone and related molecular mechanism

Arakkaveettil Kabeer Farha, Qiong Qiong Yang, Gowoon Kim, Dan Zhang, Vuyo Mavumengwana, Olivier Habimana, Hua Bin Li, Harold Corke, Ren You Gan^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

52 Scopus citations

Abstract

Staphylococcus aureus, a foodborne pathogen, poses serious problems to the food industries owing to biofilm formation, and over 25% of the foodborne illnesses in China have been attributed to S. aureus only. Phytochemicals are widely used as anti-biofilm agents with promising efficacy, and most of them are widely available and safe. This study reported the anti-biofilm efficacy of (+)-nootkatone, a sesquiterpene ketone found in a common fruit grapefruit, against multidrug-resistant S. aureus and its potential molecular mechanism. (+)-Nootkatone exhibited bacteriostatic and bactericidal effects at 200 and 400 μg/mL, respectively, against S. aureus SJTUF 20758 and S. aureus ATCC 25923. Crystal violet staining indicated that (+)-nootkatone inhibited S. aureus biofilm formation (p < 0.05) at a sub-MIC of 50 μg/mL and reduced exopolysaccharide production. The thickness of biofilms was significantly reduced by (+)-nootkatone, which was supported by the light microscopy and confocal laser scanning microscopy. Growth curve of bacteria showed that the antibacerial activity of (+)-nootkatone was dose-dependent, and the sub-MIC concentrations did not affect the bacterial growth of planktonic cells. Besides, (+)-nootkatone affected the sliding motility of S. aureus. At 200 μg/mL, (+)-nootkatone led to the reduction of preformed biofilm mass by 50% and bacterial cell death of 79%, accompanied with a reduction of exopolysaccharide. The expression of biofilm-related genes, including sarA, icaA, agrA, RNAIII, and spa, was suppressed by (+)-nootkatone, as revealed by the transcriptional analysis. Additionally, MTT assay revealed that there was no toxicity of (+)-nootkatone to the human foreskin fibroblasts (HFF) cells. Therefore, (+)-nootkatone is a promising phytochemical against S. aureus biofilms, and has the potential to be used in food industry to fight against S. aureus-induced safety issues.

Original language	English
Article number	107154
Journal	Food Control
Volume	112
DOIs	https://doi.org/10.1016/j.foodcont.2020.107154
State	Published - Jun 2020
Externally published	Yes

Keywords

(+)-Nootkatone
Biofilm
Mechanisms
Multidrug resistance
Phytochemical
Staphylococcus aureus

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.foodcont.2020.107154

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@article{4119c772fca74672bbd4168e009a0522,

title = "Inhibition of multidrug-resistant foodborne Staphylococcus aureus biofilms by a natural terpenoid (+)-nootkatone and related molecular mechanism",

abstract = "Staphylococcus aureus, a foodborne pathogen, poses serious problems to the food industries owing to biofilm formation, and over 25% of the foodborne illnesses in China have been attributed to S. aureus only. Phytochemicals are widely used as anti-biofilm agents with promising efficacy, and most of them are widely available and safe. This study reported the anti-biofilm efficacy of (+)-nootkatone, a sesquiterpene ketone found in a common fruit grapefruit, against multidrug-resistant S. aureus and its potential molecular mechanism. (+)-Nootkatone exhibited bacteriostatic and bactericidal effects at 200 and 400 μg/mL, respectively, against S. aureus SJTUF 20758 and S. aureus ATCC 25923. Crystal violet staining indicated that (+)-nootkatone inhibited S. aureus biofilm formation (p < 0.05) at a sub-MIC of 50 μg/mL and reduced exopolysaccharide production. The thickness of biofilms was significantly reduced by (+)-nootkatone, which was supported by the light microscopy and confocal laser scanning microscopy. Growth curve of bacteria showed that the antibacerial activity of (+)-nootkatone was dose-dependent, and the sub-MIC concentrations did not affect the bacterial growth of planktonic cells. Besides, (+)-nootkatone affected the sliding motility of S. aureus. At 200 μg/mL, (+)-nootkatone led to the reduction of preformed biofilm mass by 50% and bacterial cell death of 79%, accompanied with a reduction of exopolysaccharide. The expression of biofilm-related genes, including sarA, icaA, agrA, RNAIII, and spa, was suppressed by (+)-nootkatone, as revealed by the transcriptional analysis. Additionally, MTT assay revealed that there was no toxicity of (+)-nootkatone to the human foreskin fibroblasts (HFF) cells. Therefore, (+)-nootkatone is a promising phytochemical against S. aureus biofilms, and has the potential to be used in food industry to fight against S. aureus-induced safety issues.",

keywords = "(+)-Nootkatone, Biofilm, Mechanisms, Multidrug resistance, Phytochemical, Staphylococcus aureus",

author = "Farha, {Arakkaveettil Kabeer} and Yang, {Qiong Qiong} and Gowoon Kim and Dan Zhang and Vuyo Mavumengwana and Olivier Habimana and Li, {Hua Bin} and Harold Corke and Gan, {Ren You}",

note = "Publisher Copyright: {\textcopyright} 2020 Elsevier Ltd",

year = "2020",

month = jun,

doi = "10.1016/j.foodcont.2020.107154",

language = "英语",

volume = "112",

journal = "Food Control",

issn = "0956-7135",

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T1 - Inhibition of multidrug-resistant foodborne Staphylococcus aureus biofilms by a natural terpenoid (+)-nootkatone and related molecular mechanism

AU - Farha, Arakkaveettil Kabeer

AU - Yang, Qiong Qiong

AU - Kim, Gowoon

AU - Zhang, Dan

AU - Mavumengwana, Vuyo

AU - Habimana, Olivier

AU - Li, Hua Bin

AU - Corke, Harold

AU - Gan, Ren You

PY - 2020/6

Y1 - 2020/6

N2 - Staphylococcus aureus, a foodborne pathogen, poses serious problems to the food industries owing to biofilm formation, and over 25% of the foodborne illnesses in China have been attributed to S. aureus only. Phytochemicals are widely used as anti-biofilm agents with promising efficacy, and most of them are widely available and safe. This study reported the anti-biofilm efficacy of (+)-nootkatone, a sesquiterpene ketone found in a common fruit grapefruit, against multidrug-resistant S. aureus and its potential molecular mechanism. (+)-Nootkatone exhibited bacteriostatic and bactericidal effects at 200 and 400 μg/mL, respectively, against S. aureus SJTUF 20758 and S. aureus ATCC 25923. Crystal violet staining indicated that (+)-nootkatone inhibited S. aureus biofilm formation (p < 0.05) at a sub-MIC of 50 μg/mL and reduced exopolysaccharide production. The thickness of biofilms was significantly reduced by (+)-nootkatone, which was supported by the light microscopy and confocal laser scanning microscopy. Growth curve of bacteria showed that the antibacerial activity of (+)-nootkatone was dose-dependent, and the sub-MIC concentrations did not affect the bacterial growth of planktonic cells. Besides, (+)-nootkatone affected the sliding motility of S. aureus. At 200 μg/mL, (+)-nootkatone led to the reduction of preformed biofilm mass by 50% and bacterial cell death of 79%, accompanied with a reduction of exopolysaccharide. The expression of biofilm-related genes, including sarA, icaA, agrA, RNAIII, and spa, was suppressed by (+)-nootkatone, as revealed by the transcriptional analysis. Additionally, MTT assay revealed that there was no toxicity of (+)-nootkatone to the human foreskin fibroblasts (HFF) cells. Therefore, (+)-nootkatone is a promising phytochemical against S. aureus biofilms, and has the potential to be used in food industry to fight against S. aureus-induced safety issues.

AB - Staphylococcus aureus, a foodborne pathogen, poses serious problems to the food industries owing to biofilm formation, and over 25% of the foodborne illnesses in China have been attributed to S. aureus only. Phytochemicals are widely used as anti-biofilm agents with promising efficacy, and most of them are widely available and safe. This study reported the anti-biofilm efficacy of (+)-nootkatone, a sesquiterpene ketone found in a common fruit grapefruit, against multidrug-resistant S. aureus and its potential molecular mechanism. (+)-Nootkatone exhibited bacteriostatic and bactericidal effects at 200 and 400 μg/mL, respectively, against S. aureus SJTUF 20758 and S. aureus ATCC 25923. Crystal violet staining indicated that (+)-nootkatone inhibited S. aureus biofilm formation (p < 0.05) at a sub-MIC of 50 μg/mL and reduced exopolysaccharide production. The thickness of biofilms was significantly reduced by (+)-nootkatone, which was supported by the light microscopy and confocal laser scanning microscopy. Growth curve of bacteria showed that the antibacerial activity of (+)-nootkatone was dose-dependent, and the sub-MIC concentrations did not affect the bacterial growth of planktonic cells. Besides, (+)-nootkatone affected the sliding motility of S. aureus. At 200 μg/mL, (+)-nootkatone led to the reduction of preformed biofilm mass by 50% and bacterial cell death of 79%, accompanied with a reduction of exopolysaccharide. The expression of biofilm-related genes, including sarA, icaA, agrA, RNAIII, and spa, was suppressed by (+)-nootkatone, as revealed by the transcriptional analysis. Additionally, MTT assay revealed that there was no toxicity of (+)-nootkatone to the human foreskin fibroblasts (HFF) cells. Therefore, (+)-nootkatone is a promising phytochemical against S. aureus biofilms, and has the potential to be used in food industry to fight against S. aureus-induced safety issues.

KW - (+)-Nootkatone

KW - Biofilm

KW - Mechanisms

KW - Multidrug resistance

KW - Phytochemical

KW - Staphylococcus aureus

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DO - 10.1016/j.foodcont.2020.107154

M3 - 文章

AN - SCOPUS:85078998328

SN - 0956-7135

VL - 112

JO - Food Control

JF - Food Control

M1 - 107154

ER -

Inhibition of multidrug-resistant foodborne Staphylococcus aureus biofilms by a natural terpenoid (+)-nootkatone and related molecular mechanism

Abstract

Keywords

UN SDGs

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