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Antimicrobial Effect of Epigallocatechin Gallate Against Shewanella putrefaciens ATCC 8071: A Study Based on Cell Membrane and Biofilm

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Abstract

The study was to evaluate the antimicrobial impacts and biofilm influences on epigallocatechin gallate (EGCG) against Shewanella putrefaciens ATCC 8071. The minimum inhibitory concentration (MIC) of EGCG on S. putrefaciens was 160 μg mL−1. The growth curve exhibited that EGCG had a good antimicrobial activity. EGCG caused damages to the bacterial cell wall and membrane based the intracellular component leakage and cell viability analysis. The damage to the membrane integrity by EGCG has been confirmed by scanning electron microscopy (SEM) and transmission electron microscopy (TEM). SEM shows deformation of shape, TEM shows cell membrane and wall damage, and the leakage of cytoplasmic material. The treatment with EGCG at 0.25× and 0.5× MIC resulted in decreased motility and elevated levels of oxidative stress, leading to an increase in biofilm formation. These results demonstrated that EGCG may be used as a natural preservative to reduce S. putrefaciens in fish during cold storage.

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On reasonable request, the corresponding author will provide the data used or analyzed during this investigation.

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References

  1. Bian C, Cheng H, Yu H, Mei J, Xie J (2022) Effect of multi-frequency ultrasound assisted thawing on the quality of large yellow croaker (Larimichthys crocea). Ultrason Sonochem 82:105907. https://doi.org/10.1016/j.ultsonch.2021.105907

    Article  CAS  PubMed  Google Scholar 

  2. Jackson KH, Polreis JM, Tintle NL, Kris-Etherton PM, Harris WS (2019) Association of reported fish intake and supplementation status with the omega-3 index. Prostaglandins Leukot Essent Fatty Acids 142:4–10. https://doi.org/10.1016/j.plefa.2019.01.002

    Article  CAS  PubMed  Google Scholar 

  3. Mei J, Ma X, Xie J (2019) Review on natural preservatives for extending fish shelf life. Foods 8(10):490. https://doi.org/10.3390/foods8100490

    Article  CAS  PubMed Central  Google Scholar 

  4. Guo F, Liang Q, Zhang M, Chen W, Chen H, Yun Y, Zhong Q, Chen W (2021) Antibacterial activity and mechanism of linalool against Shewanella putrefaciens. Molecules 26(1):245. https://doi.org/10.3390/molecules26010245

    Article  CAS  PubMed Central  Google Scholar 

  5. Bernshteyn M, Ashok Kumar P, Joshi S (2020) Shewanella algae - A novel organism causing bacteremia: a rare case and literature review. Cureus 12(9):e10676. https://doi.org/10.7759/cureus.10676

    Article  PubMed  PubMed Central  Google Scholar 

  6. Yan F, Dang Q, Liu C, Yan J, Wang T, Fan B, Cha D, Li X, Liang S, Zhang Z (2016) 3,6-O-[N-(2-Aminoethyl)-acetamide-yl]-chitosan exerts antibacterial activity by a membrane damage mechanism. Carbohydr Polym 149:102–111. https://doi.org/10.1016/j.carbpol.2016.04.098

    Article  CAS  PubMed  Google Scholar 

  7. Nowotarska SW, Nowotarski K, Grant IR, Elliott CT, Friedman M, Situ C (2017) Mechanisms of antimicrobial action of cinnamon and oregano oils, cinnamaldehyde, carvacrol, 2,5-dihydroxybenzaldehyde, and 2-hydroxy-5-methoxybenzaldehyde against Mycobacterium avium subsp. paratuberculosis (Map). Foods 6(9):72. https://doi.org/10.3390/foods6090072

    Article  CAS  PubMed Central  Google Scholar 

  8. Zhou L, Fang L, Mei X (2019) Preservative effects of gelatin active coating enriched with eugenol emulsion on Chinese seabass (Lateolabrax maculatus) during superchilling (−0.9 °C) storage. Coatings 9(8):489. https://doi.org/10.3390/coatings9080489

    Article  CAS  Google Scholar 

  9. Li P, Zhou Q, Chu Y, Lan W, Mei J, Xie J (2020) Effects of chitosan and sodium alginate active coatings containing epsilon-polysine on qualities of cultured pufferfish (Takifugu obscurus) during cold storage. Int J Biol Macromol 160:418–428. https://doi.org/10.1016/j.ijbiomac.2020.05.092

    Article  CAS  PubMed  Google Scholar 

  10. Shokri S, Parastouei K, Taghdir M, Abbaszadeh S (2020) Application an edible active coating based on chitosan- Ferulago angulata essential oil nanoemulsion to shelf life extension of Rainbow trout fillets stored at 4 °C. Int J Biol Macromol 153:846–854. https://doi.org/10.1016/j.ijbiomac.2020.03.080

    Article  CAS  PubMed  Google Scholar 

  11. Pei J, Mei J, Wu G, Yu H, Xie J (2022) Gum tragacanth-sodium alginate active coatings containing epigallocatechin gallate reduce hydrogen peroxide content and inhibit lipid and protein oxidations of large yellow croaker (Larimichthys crocea) during superchilling storage. Food Chem 397:133792. https://doi.org/10.1016/j.foodchem.2022.133792

    Article  CAS  PubMed  Google Scholar 

  12. Gordon NC, Wareham DW (2010) Antimicrobial activity of the green tea polyphenol (-)-epigallocatechin-3-gallate (EGCG) against clinical isolates of Stenotrophomonas maltophilia. Int J Antimicrob Agents 36(2):129–131. https://doi.org/10.1016/j.ijantimicag.2010.03.025

    Article  CAS  PubMed  Google Scholar 

  13. Kitichalermkiat A, Katsuki M, Sato J, Sonoda T, Masuda Y, Honjoh KI, Miyamoto T (2020) Effect of epigallocatechin gallate on gene expression of Staphylococcus aureus. J Glob Antimicrob Resist 22:854–859. https://doi.org/10.1016/j.jgar.2020.06.006

    Article  PubMed  Google Scholar 

  14. Xu X, Zhou XD, Wu CD (2011) The tea catechin epigallocatechin gallate suppresses cariogenic virulence factors of Streptococcus mutans. Antimicrob Agents Chemother 55(3):1229–1236. https://doi.org/10.1128/AAC.01016-10

    Article  CAS  PubMed  Google Scholar 

  15. Yanagawa Y, Yamamoto Y, Hara Y, Shimamura T (2003) A combination effect of epigallocatechin gallate, a major compound of green tea catechins, with antibiotics on Helicobacter pylori growth in vitro. Curr Microbiol 47(3):244–249. https://doi.org/10.1007/s00284-002-3956-6

    Article  CAS  PubMed  Google Scholar 

  16. Asahi Y, Noiri Y, Miura J, Maezono H, Yamaguchi M, Yamamoto R, Azakami H, Hayashi M, Ebisu S (2014) Effects of the tea catechin epigallocatechin gallate on Porphyromonas gingivalis biofilms. J Appl Microbiol 116(5):1164–1171. https://doi.org/10.1111/jam.12458

    Article  CAS  PubMed  Google Scholar 

  17. Yan J, Xie J (2021) Removal of Shewanella putrefaciens biofilm by acidic electrolyzed water on food contact surfaces. Lwt 151:112044. https://doi.org/10.1016/j.lwt.2021.112044

    Article  CAS  Google Scholar 

  18. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8(9):623–633. https://doi.org/10.1038/nrmicro2415

    Article  CAS  PubMed  Google Scholar 

  19. Zhang F, Zhu J, Wang H (2016) Inhibitory activity of tea polyphenols on biofilm development of Shewanella putrefaciens. J Food Process Preserv 40(5):910–917. https://doi.org/10.1111/jfpp.12669

    Article  CAS  Google Scholar 

  20. Wang L, Zhang K, Zhang K, Zhang J, Fu J, Li J, Wang G, Qiu Z, Wang X, Li J (2020) Antibacterial activity of cinnamomum camphora essential oil on Escherichia coli during planktonic growth and biofilm formation. Front Microbiol 11:561002. https://doi.org/10.3389/fmicb.2020.561002

    Article  PubMed  PubMed Central  Google Scholar 

  21. Yan K, Wu Z, Yin Z (2018) The antibacterial mechanism of terpinen-4-ol against Streptococcus agalactiae. Curr Microbiol 75(9):1214–1220. https://doi.org/10.1007/s00284-018-1512-2

    Article  CAS  PubMed  Google Scholar 

  22. Shi C, Song K, Zhang X, Sun Y, Sui Y, Chen Y, Jia Z, Sun H, Sun Z, Xia X (2016) Antimicrobial activity and possible mechanism of action of citral against Cronobacter sakazakii. PLoS ONE 11(7):e0159006. https://doi.org/10.1371/journal.pone.0159006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Lin L, Mao X, Sun Y, Cui H (2018) Antibacterial mechanism of artemisinin/beta-cyclodextrins against methicillin-resistant Staphylococcus aureus (MRSA). Microb Pathog 118:66–73. https://doi.org/10.1016/j.micpath.2018.03.014

    Article  CAS  PubMed  Google Scholar 

  24. Cai R, Zhang M, Cui L, Yuan Y, Yang Y, Wang Z, Yue T (2019) Antibacterial activity and mechanism of thymol against Alicyclobacillus acidoterrestris vegetative cells and spores. Lwt 105:377–384. https://doi.org/10.1016/j.lwt.2019.01.066

    Article  CAS  Google Scholar 

  25. Cao J, Liu H, Wang Y, He X, Jiang H, Yao J, Xia F, Zhao Y, Chen X (2021) Antimicrobial and antivirulence efficacies of citral against foodborne pathogen Vibrio parahaemolyticus RIMD2210633. Food Control 120:107507. https://doi.org/10.1016/j.foodcont.2020.107507

    Article  CAS  Google Scholar 

  26. Yaqub A, Malkani N, Shabbir A, Ditta SA, Tanvir F, Ali S, Naz M, Kazmi SAR, Ullah R (2020) Novel biosynthesis of copper nanoparticles using Zingiber and Allium sp. with synergic effect of doxycycline for anticancer and bactericidal activity. Curr Microbiol 77(9):2287–2299. https://doi.org/10.1007/s00284-020-02058-4

    Article  CAS  PubMed  Google Scholar 

  27. Sotirova A, Avramova T, Stoitsova S, Lazarkevich I, Lubenets V, Karpenko E, Galabova D (2012) The importance of rhamnolipid-biosurfactant-induced changes in bacterial membrane lipids of Bacillus subtilis for the antimicrobial activity of thiosulfonates. Curr Microbiol 65(5):534–541. https://doi.org/10.1007/s00284-012-0191-7

    Article  CAS  PubMed  Google Scholar 

  28. Tan Z, Bo T, Guo F, Cui J, Jia S (2018) Effects of epsilon-Poly-l-lysine on the cell wall of Saccharomyces cerevisiae and its involved antimicrobial mechanism. Int J Biol Macromol 118(Pt B):2230–2236. https://doi.org/10.1016/j.ijbiomac.2018.07.094

    Article  CAS  PubMed  Google Scholar 

  29. Li R, Lu J, Duan H, Yang J, Tang C (2020) Biofilm inhibition and mode of action of epigallocatechin gallate against Vibrio mimicus. Food Control 113:107148. https://doi.org/10.1016/j.foodcont.2020.107148

    Article  CAS  Google Scholar 

  30. Zhang Y, Wu Y-T, Zheng W, Han X-X, Jiang Y-H, Hu P-L, Tang Z-X, Shi L-E (2017) The antibacterial activity and antibacterial mechanism of a polysaccharide from Cordyceps cicadae. J Funct Foods 38:273–279. https://doi.org/10.1016/j.jff.2017.09.047

    Article  CAS  Google Scholar 

  31. Yan J, Xie J (2020) Comparative proteome analysis of Shewanella putrefaciens WS13 mature biofilm under cold stress. Front Microbiol 11:1225. https://doi.org/10.3389/fmicb.2020.01225

    Article  PubMed  PubMed Central  Google Scholar 

  32. Zhang N, Lan W, Wang Q, Sun X, Xie J (2018) Antibacterial mechanism of Ginkgo biloba leaf extract when applied to Shewanella putrefaciens and Saprophytic staphylococcus. Aquac Fish 3(4):163–169. https://doi.org/10.1016/j.aaf.2018.05.005

    Article  Google Scholar 

  33. Lan W, Zhang N, Liu S, Chen M, Xie J (2019) ε-polylysine inhibits Shewanella putrefaciens with membrane disruption and cell damage. Molecules 24(20):3727. https://doi.org/10.3390/molecules24203727

    Article  CAS  PubMed Central  Google Scholar 

  34. Xu D, Sun L, Li C, Wang Y (2018) Ye R (2018) Inhibitory effect of glucose oxidase from Bacillus sp. CAMT22370 on the quality deterioration of Pacific white shrimp during cold storage. LWT 92:339–346. https://doi.org/10.1016/j.lwt.2018.02.025

    Article  CAS  Google Scholar 

  35. Kos G, Lohninger H, Krska R (2003) Development of a method for the determination of fusarium fungi on corn using mid-infrared spectroscopy with attenuated total reflection and chemometrics. Anal Chem 75(5):1211–1217. https://doi.org/10.1021/ac0260903

    Article  CAS  PubMed  Google Scholar 

  36. Guo Z-Y, Zhang Z-Y, Xiao J-Q, Qin J-H, Zhao W (2018) Antibacterial effects of leaf extract of Nandina domestica and the underlined mechanism. Evid Based Complementary Altern Med 2018:1–9. https://doi.org/10.1155/2018/8298151

    Article  Google Scholar 

  37. Nakonieczna J, Michta E, Rybicka M, Grinholc M, Gwizdek-Wisniewska A, Bielawski KP (2010) Superoxide dismutase is upregulated in Staphylococcus aureus following protoporphyrin-mediated photodynamic inactivation and does not directly influence the response to photodynamic treatment. BMC Microbiol 10:323. https://doi.org/10.1186/1471-2180-10-323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Brown II, Hase CC (2001) Flagellum-independent surface migration of Vibrio cholerae and Escherichia coli. J Bacteriol 183(12):3784–3790. https://doi.org/10.1128/JB.183.12.3784-3790.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Wang F, Wei F, Song C, Jiang B, Tian S, Yi J, Yu C, Song Z, Sun L, Bao Y, Wu Y, Huang Y, Li Y (2017) Dodartia orientalis L. essential oil exerts antibacterial activity by mechanisms of disrupting cell structure and resisting biofilm. Ind Crops Prod 109:358–366. https://doi.org/10.1016/j.indcrop.2017.08.058

    Article  CAS  Google Scholar 

  40. Liu W, Mei J, Xie J (2020) Elucidating antibacterial activity and mechanism of daphnetin against Pseudomonas fluorescens and Shewanella putrefaciens. J Food Qual 2020:1–10. https://doi.org/10.1155/2020/6622355

    Article  CAS  Google Scholar 

  41. Zhao L, Zhang H, Hao T, Li S (2015) In vitro antibacterial activities and mechanism of sugar fatty acid esters against five food-related bacteria. Food Chem 187:370–377. https://doi.org/10.1016/j.foodchem.2015.04.108

    Article  CAS  PubMed  Google Scholar 

  42. Yu H, Pei J, Qiu W, Mei J, Xie J (2022) The antimicrobial effect of Melissa officinalis L. essential oil on Vibrio parahaemolyticus: insights based on the cell membrane and external structure. Front Microbiol 13. https://doi.org/10.3389/fmicb.2022.812792

  43. Salman A, Shufan E, Sharaha U, Lapidot I, Mordechai S, Huleihel M (2019) Distinction between mixed genus bacteria using infrared spectroscopy and multivariate analysis. Vib Spectrosc 100:6–13. https://doi.org/10.1016/j.vibspec.2018.10.009

    Article  CAS  Google Scholar 

  44. Lee DS, Je JY (2013) Gallic acid-grafted-chitosan inhibits foodborne pathogens by a membrane damage mechanism. J Agric Food Chem 61(26):6574–6579. https://doi.org/10.1021/jf401254g

    Article  CAS  PubMed  Google Scholar 

  45. Deng H, Zhu J, Tong Y, Kong Y, Tan C, Wang M, Wan M, Meng X (2021) Antibacterial characteristics and mechanisms of action of Aronia melanocarpa anthocyanins against Escherichia coli. Lwt 150:112018. https://doi.org/10.1016/j.lwt.2021.112018

    Article  CAS  Google Scholar 

  46. Xiong LG, Chen YJ, Tong JW, Huang JA, Li J, Gong YS, Liu ZH (2017) Tea polyphenol epigallocatechin gallate inhibits Escherichia coli by increasing endogenous oxidative stress. Food Chem 217:196–204. https://doi.org/10.1016/j.foodchem.2016.08.098

    Article  CAS  PubMed  Google Scholar 

  47. Rosseti IB, Rocha JB, Costa MS (2015) Diphenyl diselenide (PhSe)2 inhibits biofilm formation by Candida albicans, increasing both ROS production and membrane permeability. J Trace Elem Med Biol 29:289–295. https://doi.org/10.1016/j.jtemb.2014.08.001

    Article  CAS  PubMed  Google Scholar 

  48. Geier H, Mostowy S, Cangelosi GA, Behr MA, Ford TE (2008) Autoinducer-2 triggers the oxidative stress response in Mycobacterium avium, leading to biofilm formation. Appl Environ Microbiol 74(6):1798–1804. https://doi.org/10.1128/aem.02066-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. O’May C, Ciobanu A, Lam H, Tufenkji N (2012) Tannin derived materials can block swarming motility and enhance biofilm formation in Pseudomonas aeruginosa. Biofouling 28(10):1063–1076. https://doi.org/10.1080/08927014.2012.725130

    Article  CAS  PubMed  Google Scholar 

  50. Bikels-Goshen T, Landau E, Saguy S, Shapira R (2010) Staphylococcal strains adapted to epigallocathechin gallate (EGCG) show reduced susceptibility to vancomycin, oxacillin and ampicillin, increased heat tolerance, and altered cell morphology. Int J Food Microbiol 138(1–2):26–31. https://doi.org/10.1016/j.ijfoodmicro.2010.01.011

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Dr Zhengkai Yi, College of Food Science and Technology, Shanghai Ocean University, Shanghai, China for his critical review of this manuscript.

Funding

This research was financially supported by National Natural Science Foundation of China (grant number: 31972142), Shanghai Municipal Science and technology project to enhance the capabilities of the platform (20DZ2292200, 19DZ2284000).

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JP and JM: Conceptualization; JP and HY: Data curation; JP and HY: Formal analysis; JX: Funding acquisition; JP and JM: Investigation; JP, JM, WQ and JX: Methodology; JM and JX: Project administration; JP and WQ: Software; JX: Validation; JP and JM: Writing-original draft; JM and JX: Writing-review & editing.

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Correspondence to Jun Mei or Jing Xie.

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Pei, J., Yu, H., Qiu, W. et al. Antimicrobial Effect of Epigallocatechin Gallate Against Shewanella putrefaciens ATCC 8071: A Study Based on Cell Membrane and Biofilm. Curr Microbiol 79, 297 (2022). https://doi.org/10.1007/s00284-022-02978-3

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