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. 2021 Jun 2:12:679808.
doi: 10.3389/fmicb.2021.679808. eCollection 2021.

Inactivation Effect of Thymoquinone on Alicyclobacillus acidoterrestris Vegetative Cells, Spores, and Biofilms

Qiuxia Fan  1   2 , Cheng Liu  1   2 , Zhenpeng Gao  1   2 , Zhongqiu Hu  1   2 , Zhouli Wang  1   2 , Jianbo Xiao  3 , Yahong Yuan  1   2 , Tianli Yue  1   2   4
Affiliations

Inactivation Effect of Thymoquinone on Alicyclobacillus acidoterrestris Vegetative Cells, Spores, and Biofilms

Qiuxia Fan et al. Front Microbiol. .

Abstract

Alicyclobacillus acidoterrestris (A. acidoterrestris), a spore-forming bacterium, has become a main challenge and concern for the juices and acid beverage industry across the world due to its thermo-acidophilic characteristic. Thymoquinone (TQ) is one of the active components derived from Nigella sativa seeds. The objective of this study was to investigate antibacterial activity and associated molecular mechanism of TQ against A. acidoterrestris vegetative cells, and to evaluate effects of TQ on A. acidoterrestris spores and biofilms formed on polystyrene and stainless steel surfaces. Minimum inhibitory concentrations of TQ against five tested A. acidoterrestris strains ranged from 32 to 64 μg/mL. TQ could destroy bacterial cell morphology and membrane integrity in a concentration-dependent manner. Field-emission scanning electron microscopy observation showed that TQ caused abnormal morphology of spores and thus exerted a killing effect on spores. Moreover, TQ was effective in inactivating and removing A. acidoterrestris mature biofilms. These findings indicated that TQ is promising as a new alternative to control A. acidoterrestris and thereby reduce associated contamination and deterioration in the juice and acid beverage industry.

Keywords: Alicyclobacillus acidoterrestris; Nigella sativa; biofilm; inactivation effect; spore-forming bacteria; spores; thymoquinone.

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Conflict of interest statement

The 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
Growth curves (A) of A. acidoterrestris DSM 3922 in the presence of TQ (1 × MIC∼1/16 × MIC). Time-kill curves (B) of TQ (0, 1/2 × MIC, 1 × MIC, and 2 × MIC) against A. acidoterrestris DSM 3922 in AAM broth. Error bars represent standard deviation of three replicates. OD 600 nm, optical density at 600 nm.
FIGURE 2
FIGURE 2
Scanning electronic images of A. acidoterrestris DSM 3922 after exposure to TQ of 0 (control), 1 × MIC and 2 × MIC for 2 h.
FIGURE 3
FIGURE 3
Confocal laser scanning microscopy images of A. acidoterrestris DSM 3922 after treatment with TQ of 0 (control), 1 × MIC and 2 × MIC for 60 min. Scale bar: 10 μm.
FIGURE 4
FIGURE 4
Inactivation effect of TQ on A. acidoterrestris spores. The spores were treated with TQ at the concentrations of 0 (control), 4 × MIC, 8 × MIC, and 16 × MIC for 360 min. Error bars represent standard deviation of three replicates.
FIGURE 5
FIGURE 5
Scanning electronic images of A. acidoterrestris DSM 3922 spores after treatment with TQ of 0 (control), 4 × MIC, 8 × MIC, and 16 × MIC for 6 h.
FIGURE 6
FIGURE 6
Inactivation effect of TQ on A. acidoterrestris DSM 3922 biofilms grown in AAM broth at 45°C for 24 h on polystyrene (A) and stainless steel (B) surfaces. Formed biofilms were treated with TQ at the concentrations of 0 (control), 2 × MIC, 4 × MIC, and 8 × MIC for 180 min. Error bars represent standard deviation of three replicates.
FIGURE 7
FIGURE 7
Scanning electronic images of A. acidoterrestris DSM 3922 biofilms after exposure to TQ of 0 (control), 2 × MIC, 4 × MIC, and 8 × MIC for 4 h.
See this image and copyright information in PMC

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