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Applied microbiology and biotechnology
Jun, 2021;105 (11): 4709-4718.

Antimicrobial and anti-biofilm activity of thymoquinone against Shigella flexneri.

Qiuxia Fan, Yahong Yuan, Hang Jia, Xuejun Zeng, Zhouli Wang, Zhongqiu Hu, Zhenpeng Gao, Tianli Yue
Author Information
  1. Qiuxia Fan: College of Food Science and Engineering, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.
  2. Yahong Yuan: College of Food Science and Engineering, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.
  3. Hang Jia: College of Food Science and Engineering, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.
  4. Xuejun Zeng: College of Food Science and Engineering, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.
  5. Zhouli Wang: College of Food Science and Engineering, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.
  6. Zhongqiu Hu: College of Food Science and Engineering, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.
  7. Zhenpeng Gao: College of Food Science and Engineering, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.
  8. Tianli Yue: College of Food Science and Engineering, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China. yuetl305@nwsuaf.edu.cn. ORCID
PMID: 34014346 DOI: 10.1007/s00253-021-11295-x

Abstract

Shigella flexneri (Sh. flexneri), a common foodborne pathogen, has become one of the main threats to food safety and human health due to its high pathogenicity and persistent infection. The objective of this study was to explore the antimicrobial and anti-biofilm activities and the possible mechanism of thymoquinone (TQ) against Sh. flexneri. The minimum inhibitory concentration (MIC) and minimal bactericidal concentration (MBC) of TQ against Sh. flexneri were 0.4 and 0.5 mg/mL, respectively. TQ showed bactericidal activity against Sh. flexneri in culture medium and milk system. Scanning electron microscopy (SEM) and confocal laser scanning microscopy (CLSM) observations demonstrated that TQ could induce abnormal cell morphology and destroy cell membrane. Sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS-PAGE) analysis suggested that TQ could inhibit protein synthesis in Sh. flexneri. Also, at sub-inhibitory concentrations (SICs), TQ exhibited an inhibitory effect on Sh. flexneri biofilm formation, which was confirmed by crystal violet quantitative analysis and SEM observation. Real-time quantitative PCR (RT-qPCR) analyses revealed that TQ downregulated the expression of genes involved in Sh. flexneri biofilm formation. Thus, TQ has potential as a natural antimicrobial and anti-biofilm agent to address the contamination and infection caused by Sh. flexneri. KEY POINTS: • Antimicrobial and anti-biofilm activity of TQ on Shigella flexneri were investigated. • TQ inhibited biofilm formation by Shigella flexneri. • TQ provided a new strategy for Shigella flexneri control.

Keywords

Antimicrobial Biofilm formation Shigella flexneri Thymoquinone

References

  1. Adnan M, Patel M, Deshpande S, Alreshidi M, Siddiqui AJ, Reddy MN, Emira N, De FV (2020) Effect of Adiantum philippense extract on biofilm formation, adhesion with its antibacterial activities against foodborne pathogens, and characterization of bioactive metabolites: an in vitro-in silico approach. Front Microbiol 11:823. https://doi.org/10.3389/fmicb.2020.00823 [DOI: 10.3389/fmicb.2020.00823]
  2. Ahmed AM, Shimamoto T (2015) Molecular characterization of multidrug-resistant Shigella spp. of food origin. Int J Food Microbiol 194:78–82. https://doi.org/10.1016/j.ijfoodmicro.2014.11.013 [DOI: 10.1016/j.ijfoodmicro.2014.11.013]
  3. Al-Majed AA, Al-Omar FA, Nagi MN (2006) Neuroprotective effects of thymoquinone against transient forebrain ischemia in the rat hippocampus. Eur J Pharmacol 543(1-3):40–47. https://doi.org/10.1016/j.ejphar.2006.05.046 [DOI: 10.1016/j.ejphar.2006.05.046]
  4. Bridier A, Sanchez-Vizuete P, Guilbaud M, Piard JC, Naitali M, Briandet R (2015) Biofilm-associated persistence of food-borne pathogens. Food Microbiol 45(Pt B):167–178. https://doi.org/10.1016/j.fm.2014.04.015 [DOI: 10.1016/j.fm.2014.04.015]
  5. Chimnoi N, Reuk-Ngam N, Chuysinuan P, Khlaychan P, Khunnawutmanotham N, Chokchaichamnankit D, Thamniyom W, Klayraung S, Mahidol C, Techasakul S (2018) Characterization of essential oil from Ocimum gratissimum leaves: antibacterial and mode of action against selected gastroenteritis pathogens. Microb Pathog 118:290–300. https://doi.org/10.1016/j.micpath.2018.03.041 [DOI: 10.1016/j.micpath.2018.03.041]
  6. Costa JG, Keser V, Jackson C, Saraiva N, Guerreiro I, Almeida N, Camoes SP, Manguinhas R, Castro M, Fernandes AS, Oliveira NG (2020) A multiple endpoint approach reveals potential in vitro anticancer properties of thymoquinone in human renal carcinoma cells. Food Chem Toxicol 136:111076. https://doi.org/10.1016/j.fct.2019.111076 [DOI: 10.1016/j.fct.2019.111076]
  7. Coughlan LM, Cotter PD, Hill C, Alvarez-Ordonez A (2016) New weapons to fight old enemies: novel strategies for the (bio)control of bacterial biofilms in the food industry. Front Microbiol 7:1641. https://doi.org/10.3389/fmicb.2016.01641 [DOI: 10.3389/fmicb.2016.01641]
  8. Diao WR, Hu QP, Zhang H, Xu JG (2014) Chemical composition, antibacterial activity and mechanism of action of essential oil from seeds of fennel (Foeniculum vulgare Mill.). Food Control 35(1):109–116. https://doi.org/10.1016/j.foodcont.2013.06.056 [DOI: 10.1016/j.foodcont.2013.06.056]
  9. El Gazzar M, El Mezayen R, Marecki JC, Nicolls MR, Canastar A, Dreskin SC (2006) Anti-inflammatory effect of thymoquinone in a mouse model of allergic lung inflammation. Int Immunopharmacol 6(7):1135–1142. https://doi.org/10.1016/j.intimp.2006.02.004 [DOI: 10.1016/j.intimp.2006.02.004]
  10. Frankova A, Marounek M, Mozrova V, Weber J, Kloucek P, Lukesova D (2014) Antibacterial activities of plant-derived compounds and essential oils toward Cronobacter sakazakii and Cronobacter malonaticus. Foodborne Pathog Dis 11(10):795–797. https://doi.org/10.1089/fpd.2014.1737 [DOI: 10.1089/fpd.2014.1737]
  11. Gu H, Fan D, Gao J, Zou W, Peng Z, Zhao Z, Ling J, LeGeros RZ (2012) Effect of ZnCl2 on plaque growth and biofilm vitality. Arch Oral Biol 57(4):369–375. https://doi.org/10.1016/j.archoralbio.2011.10.001 [DOI: 10.1016/j.archoralbio.2011.10.001]
  12. Halawani E (2009) Antibacterial activity of thymoquinone and thymohydroquinone of Nigella sativa L. and their interaction with some antibiotics.Advan. Biol Res 3(5-6):148–152
  13. Hirudkar JR, Parmar KM, Prasad RS, Sinha SK, Jogi MS, Itankar PR, Prasad SK (2020) Quercetin a major biomarker of Psidium guajava L. inhibits SepA protease activity of Shigella flexneri in treatment of infectious diarrhoea. Microb. Pathogenesis 138:103807. https://doi.org/10.1016/j.micpath.2019.103807 [DOI: 10.1016/j.micpath.2019.103807]
  14. Huang JF, Yang LY, Zou Y, Luo SC, Wang X, Liang YJ, Du YH, Feng RZ, Wei Q (2021) Antibacterial activity and mechanism of three isomeric terpineols of Cinnamomum longepaniculatum leaf oil. Folia Microbiol 66(1):59–67. https://doi.org/10.1007/s12223-020-00818-0 [DOI: 10.1007/s12223-020-00818-0]
  15. Kalus U, Pruss A, Bystron J, Jurecka M, Smekalova A, Lichius JJ, Kiesewetter H (2003) Effect of Nigella sativa (black seed) on subjective feeling in patients with allergic diseases. Phytother Res 17(10):1209–1214. https://doi.org/10.1002/ptr.1356 [DOI: 10.1002/ptr.1356]
  16. Kang J, Liu L, Liu M, Wu X, Li J (2018a) Antibacterial activity of gallic acid against Shigella flexneri and its effect on biofilm formation by repressing mdoH gene expression. Food Control 94:147–154.  https://doi.org/10.1016/j.foodcont.2018.07.011
  17. Kang J, Liu L, Liu Y, Wang X (2020) Ferulic acid inactivates Shigella flexneri through cell membrane destruction, biofilm retardation, and altered gene expression. J Agric Food Chem 68(27):7121–7131. https://doi.org/10.1021/acs.jafc.0c01901 [DOI: 10.1021/acs.jafc.0c01901]
  18. Kang J, Liu L, Wu X, Sun Y, Liu Z (2018b) Effect of thyme essential oil against Bacillus cereus planktonic growth and biofilm formation. Appl Microbiol Biotechnol 102(23):10209–10218. https://doi.org/10.1007/s00253-018-9401-y [DOI: 10.1007/s00253-018-9401-y]
  19. Liu F, Wang F, Du L, Zhao T, Doyle MP, Wang D, Zhang X, Sun Z, Xu W (2018) Antibacterial and antibiofilm activity of phenyllactic acid against Enterobacter cloacae. Food Control 84:442–448. https://doi.org/10.1016/j.foodcont.2017.09.004 [DOI: 10.1016/j.foodcont.2017.09.004]
  20. Livio S, Strockbine NA, Panchalingam S, Tennant SM, Barry EM, Marohn ME, Antonio M, Hossain A, Mandomando I, Ochieng JB, Oundo JO, Qureshi S, Ramamurthy T, Tamboura B, Adegbola RA, Hossain MJ, Saha D, Sen S, Faruque AS, Alonso PL, Breiman RF, Zaidi AK, Sur D, Sow SO, Berkeley LY, O'Reilly CE, Mintz ED, Biswas K, Cohen D, Wu Y, Blackwelder WC, Kotloff KL, Nataro JP, Levine MM (2014) Shigella isolates from the global enteric multicenter study inform vaccine development. Clin Infect Dis 59(7):933–941. https://doi.org/10.1093/cid/ciu468 [DOI: 10.1093/cid/ciu468]
  21. Miao X, Liu H, Zheng Y, Guo D, Shi C, Xu Y, Xia X (2019) Inhibitory effect of thymoquinone on Listeria monocytogenes ATCC 19115 biofilm formation and virulence attributes critical for human infection. Front Cell Infect Microbiol 9:304. https://doi.org/10.3389/fcimb.2019.00304 [DOI: 10.3389/fcimb.2019.00304]
  22. Ngome MT, Alves J, de Oliveira ACF, da Silva MP, Mondragon-Bernal OL, Piccoli RH (2018) Linalool, citral, eugenol and thymol: control of planktonic and sessile cells of Shigella flexneri. AMB Express 8(1):105. https://doi.org/10.1186/s13568-018-0634-z [DOI: 10.1186/s13568-018-0634-z]
  23. Nickerson KP, Chanin RB, Sistrunk JR, Rasko DA, Fink PJ, Barry EM, Nataro JP, Faherty CS (2017) Analysis of Shigella flexneri resistance, biofilm formation, and transcriptional profile in response to bile salts. Infect Immun 85(6):e01067–e01016. https://doi.org/10.1128/IAI.01067-16 [DOI: 10.1128/IAI.01067-16]
  24. Rahimi E, Shirazi F, Khamesipour F (2017) Isolation and study of the antibiotic resistance properties of Shigella species in meat and meat products. J Food Process Preserv 41(3):e12947. https://doi.org/10.1111/jfpp.12947 [DOI: 10.1111/jfpp.12947]
  25. Rohinishree YS, Negi PS (2016) Effect of licorice extract on cell viability, biofilm formation and exotoxin production by Staphylococcus aureus. J Food Sci Technol 53(2):1092–1100. https://doi.org/10.1007/s13197-015-2131-6 [DOI: 10.1007/s13197-015-2131-6]
  26. Shahin K, Bouzari M, Wang R, Yazdi M (2019) Prevalence and molecular characterization of multidrug-resistant Shigella species of food origins and their inactivation by specific lytic bacteriophages. Int J Food Microbiol 305:108252. https://doi.org/10.1016/j.ijfoodmicro.2019.108252 [DOI: 10.1016/j.ijfoodmicro.2019.108252]
  27. Shi C, Zhao X, Yan H, Meng R, Zhang Y, Li W, Liu Z, Guo N (2016) Effect of tea tree oil on Staphylococcus aureus growth and enterotoxin production. Food Control 62:257–263. https://doi.org/10.1016/j.foodcont.2015.10.049 [DOI: 10.1016/j.foodcont.2015.10.049]
  28. Silva-Angulo AB, Zanini SF, Rosenthal A, Rodrigo D, Klein G, Martinez A (2015) Comparative study of the effects of citral on the growth and injury of Listeria innocua and Listeria monocytogenes cells. PLoS One 10(2):e0114026. https://doi.org/10.1371/journal.pone.0114026 [DOI: 10.1371/journal.pone.0114026]
  29. Song Y, Sun M, Feng L, Liang X, Song X, Mu G, Tuo Y, Jiang S, Qian F (2020) Antibiofilm activity of Lactobacillus plantarum 12 exopolysaccharides against Shigella flexneri. Appl Environ Microbiol 86(15). https://doi.org/10.1128/aem.00694-20
  30. Ulasli SS, Celik S, Gunay E, Ozdemir M, Hazman O, Ozyurek A, Koyuncu T, Unlu M (2013) Anticancer effects of thymoquinone, caffeic acid phenethyl ester and resveratrol on A549 non-small cell lung cancer cells exposed to benzo(a)pyrene. Asian Pac J Cancer Prev 14(10):6159–6164. https://doi.org/10.7314/apjcp.2013.14.10.6159 [DOI: 10.7314/apjcp.2013.14.10.6159]
  31. Wang C, Chang T, Yang H, Cui M (2015) Antibacterial mechanism of lactic acid on physiological and morphological properties of Salmonella enteritidis, Escherichia coli and Listeria monocytogenes. Food Control 47:231–236. https://doi.org/10.1016/j.foodcont.2014.06.034 [DOI: 10.1016/j.foodcont.2014.06.034]
  32. Zheng X, Guo J, Rao H, Guo D, Huang Y, Xu Y, Liang S, Xia X, Shi C (2020) Antibacterial and antibiofilm activity of coenzyme Q0 against Vibrio parahaemolyticus. Food Control 109:106955. https://doi.org/10.1016/j.foodcont.2019.106955 [DOI: 10.1016/j.foodcont.2019.106955]

Grants

  1. 2019YFC1606703/National Key Research and Development Project During the 13th Five-Year Plan

MeSH Term

Anti-Bacterial Agents
Benzoquinones
Biofilms
Humans
Shigella flexneri

Chemicals

Anti-Bacterial Agents
Benzoquinones
thymoquinone
Journal Article
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