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. 2024 Nov 28;13(23):3841.
doi: 10.3390/foods13233841.

Anti-Bacterial and Anti-Biofilm Activities of Essential Oil from Citrus reticulata Blanco cv. Tankan Peel Against Listeria monocytogenes

Jinming Peng  1   2 , Guangwei Chen  1   2 , Shaoxin Guo  1   2 , Ziyuan Lin  1   2 , Yue Zeng  1   2 , Jie Ren  3 , Qin Wang  1   2 , Wenhua Yang  1   2 , Yongqian Liang  4 , Jun Li  1   2
Affiliations

Anti-Bacterial and Anti-Biofilm Activities of Essential Oil from Citrus reticulata Blanco cv. Tankan Peel Against Listeria monocytogenes

Jinming Peng et al. Foods. .

Abstract

In recent years, plant essential oils have been confirmed as natural inhibitors of foodborne pathogens. Citrus reticulata Blanco cv. Tankan peel essential oil (CPEO) showed anti-Listeria monocytogenes (LM) activities, and this study investigated the associated mechanisms by using high-resolution electron microscope, fluorescence spectrometer, flow cytometer, potentiometer, and transcriptome sequencing. The results showed that CPEO restrained LM growth at a minimum inhibitory concentration of 2% (v/v). The anti-LM abilities of CPEO were achieved by disrupting the permeability of the cell wall, damaging the permeability, fluidity, and integrity of the cell membrane, disturbing the membrane hydrophobic core, and destroying the membrane protein conformation. Moreover, CPEO could significantly inhibit the LM aggregation from forming biofilm by reducing the extracellular polymeric substances' (protein, polysaccharide, and eDNA) production and bacterial surface charge numbers. The RNA sequencing data indicated that LM genes involved in cell wall and membrane biosynthesis, DNA replication and repair, quorum sensing and two-component systems were expressed differently after CPEO treatment. These results suggested that CPEO could be used as a novel anti-LM agent and green preservative in the food sector. Further studies are needed to verify the anti-LM activities of CPEO in real food.

Keywords: Listeria monocytogenes; biofilm; cell membrane; essential oils; extracellular polymeric substances; transcriptome analysis.

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Conflict of interest statement

Author Jie Ren was employed by the company Nuspower Greatsun (Guangdong) Biotechnology Co., Ltd. He participated in conceptualization, validation, and investigation in the study. The role of the company was Vice president of R&D. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Minimum inhibitory concentration of Citrus reticulata Blanco cv. Tankan peel essential oil (CPEO) on LM (A). Growth curvatures of LM with and without exposure to CPEO (B). Columns marked with different letters imply that the differences are statistically significant (p < 0.05).
Figure 2
Figure 2
SEM micrographs of untreated LM (A) and Citrus reticulata Blanco cv. Tankan peel essential oil (CPEO)-treated LM (B). TEM images of untreated LM (C) and CPEO-treated LM (D).
Figure 3
Figure 3
Alkaline phosphatase (AKP) (A) and protein (B) leakage from LM treated with or without Citrus reticulata Blanco cv. Tankan peel essential oil (CPEO). Cell membrane fluidity (C) and integrity (D) of LM treated with or without CPEO. Columns marked with different letters imply that the differences are statistically significant (p < 0.05).
Figure 4
Figure 4
Exploring the effects of Citrus reticulata Blanco cv. Tankan peel essential oil (CPEO) on the cell membrane structure by using in vitro POPG liposome. Effects of CPEO on fluorescent spectrum of liposome tagged with various probes including NBD-PE (A), TMA-DPH (B), and DPH (C). The fluorescence quenching of various probes after CPEO treatment (D). Columns marked with different letters imply that the differences are statistically significant (p < 0.05).
Figure 5
Figure 5
The membrane protein conformation of LM treated with or without Citrus reticulata Blanco cv. Tankan peel essential oil (CPEO). The variations in the fluorescent spectrum of the particular amino acids include Tyr (A), Trp (B), and Phe (C) in the membrane protein.
Figure 6
Figure 6
Biofilm formation curves of LM treated with or without Citrus reticulata Blanco cv. Tankan peel essential oil (CPEO) (A). Aggregation ability of LM treated with or without CPEO (B). Influences of CPEO on EPS (protein, PRO; polysaccharide, POL; eDNA) production of LM biofilm (C). Effects of CPEO on the surface charge of LM (D). Columns marked with different letters imply that differences are statistically significant (p < 0.05).
Figure 7
Figure 7
Transcriptomic profiles of Citrus reticulata Blanco cv. Tankan peel essential oil (CPEO)-treated LM in comparison to the control group (CON). (A) Numbers of up-regulated and down-regulated differentially expressed genes (DEGs). (B) Volcano plot analysis of DEGs in LM. (C) GO enrichment analysis categorizing DEGs into molecular function (MF), biological process (BP), and cellular component (CC). (D) KEGG enrichment bubble chart of DEGs. The larger the bubble, the greater the quantity, and the redder the bubble, the lower the P-value/Q-value ratio.
Figure 8
Figure 8
Heatmaps depicting representative DEGs related to cell wall synthesis and cell membrane integrity in LM, including peptidoglycan biosynthesis, amino sugar and nucleotide sugar metabolism, sucrose metabolism, glycerolipid metabolism and glycerophospholipid metabolism. Red denotes gene up-regulation while blue denotes gene down-regulation; the darker the color, the greater the change.
Figure 9
Figure 9
Heatmaps depicting the representative DEGs related to DNA replication and repair in LM. Red denotes gene up-regulation while blue denotes gene down-regulation; the darker the color, the greater the change.
Figure 10
Figure 10
Heatmaps depicting the representative DEGs related to the quorum sensing system and two-component system in LM. Red denotes gene up-regulation while blue denotes gene down-regulation; the darker the color, the greater the change.
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