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Antimicrobial Activity of Natural Plant Compound Carvacrol Against Soft Rot Disease Agent Dickeya zeae

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Abstract

Dickeya zeae is a globally important bacterial pathogen that has been reported to cause severe soft rot diseases in several essential food crops, including bananas, rice, maize, and potatoes. Carvacrol, a hydrophobic terpene component, is found in aromatic plants of the Labiatae family and various essential oils. However, little work has been done on its antimicrobial potential against D. zeae. This study aimed to evaluate the antimicrobial activity and the functional mechanism of carvacrol against D. zeae. The minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) of carvacrol against D. zeae were 0.1 mg/mL and 0.2 mg/mL, respectively. Carvacrol affected the cell membrane of D. zeae, as revealed by decreased intracellular ATP concentration, nucleic acid leakage, and decreased membrane potential. Scanning electron microscopy (SEM) micrographs confirmed that D. zeae cell membranes were damaged by carvacrol. Furthermore, a significant inhibition of D. zeae swimming motility and biofilm formation was observed following treatments with carvacrol at sub-inhibitory concentrations, indicating a significantly negative effect on these virulence factors. Accordingly, the tissue infection test revealed that carvacrol significantly reduced the pathogenicity of D. zeae. In a pot experiment, inoculated banana seedlings displayed remarkably lesser disease symptoms following treatment with carvacrol, and the control efficiency for banana soft rot was 32.0% at 14 days post-inoculation. To summarize, carvacrol exhibits strong antimicrobial activity against D. zeae and great potential applications in the control of D. zeae-associated crop diseases.

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References

  1. Gardan L (2005) Transfer of Pectobacterium chrysanthemi (Burkholder et al. 1953) Brenner et al. 1973 and Brenneria paradisiaca to the genus Dickeya gen. nov. as Dickeya chrysanthemi comb. nov. and Dickeya paradisiaca comb. nov. and delineation of four novel species, Dickeya dadantii sp. nov., Dickeya dianthicola sp. nov., Dickeya dieffenbachiae sp. nov. and Dickeya zeae sp. nov. Int J Syst Evol Microbiol 55(1):1415–1427. https://doi.org/10.1099/ijs.0.02791-0

    Article  CAS  PubMed  Google Scholar 

  2. Hu M, Li J, Chen R, Li W, Feng L, Shi L, Xue Y, Feng X, Zhang L, Zhou J (2018) Dickeya zeae strains isolated from rice, banana and clivia rot plants show great virulence differentials. BMC Microbiol 18:136. https://doi.org/10.1186/s12866-018-1300-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Li J, Hu M, Xue Y, Chen X, Lu G, Zhang L, Zhou J (2020) Screening, identification and efficacy evaluation of antagonistic bacteria for biocontrol of soft rot disease caused by Dickeya zeae. Microorganisms 8:697. https://doi.org/10.3390/microorganisms8050697

    Article  CAS  PubMed Central  Google Scholar 

  4. Lin B, Shen H, Pu X, Tian X, Zhao W, Zhu S, Dong M (2010) First report of a soft rot of banana in mainland China caused by a Dickeya sp. (Pectobacterium chrysanthemi). Plant Dis 94:640–640. https://doi.org/10.1094/PDIS-94-5-0640C

    Article  CAS  PubMed  Google Scholar 

  5. Zhang J, Shen H, Pu X, Lin B, Hu J (2014) Identification of Dickeya zeae as a causal agent of bacterial soft rot in banana in China. Plant Dis 98:436–442. https://doi.org/10.1094/PDIS-07-13-0711-RE

    Article  CAS  PubMed  Google Scholar 

  6. Czajkowski R, Perombelon M, Jafra S, Lojkowska E, Potrykus M, van der Wolf J, Sledz W (2015) Detection, identification and differentiation of Pectobacterium and Dickeya species causing potato blackleg and tuber soft rot: a review. Ann Appl Biol 166:18–38. https://doi.org/10.1111/aab.12166

    Article  CAS  PubMed  Google Scholar 

  7. Bogino PC, Oliva MDlM, Sorroche FG, Giordano W (2013) The role of bacterial biofilms and surface components in plant-bacterial associations. Int J Mol Sci 14:15838–15859. https://doi.org/10.3390/ijms140815838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P, Dow M, Verdier V, Beer SV, Machado MA (2012) Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 13:614–629. https://doi.org/10.1111/j.1364-3703.2012.00804.x

    Article  PubMed  PubMed Central  Google Scholar 

  9. Huang N, Pu X, Zhang J, Shen H, Yang Q, Wang Z, Lin B (2019) In vitro formation of Dickeya zeae MS1 biofilm. Curr Microbiol 76:100–107. https://doi.org/10.1007/s00284-018-1593-y

    Article  CAS  PubMed  Google Scholar 

  10. Wu J, Song Z, Xiang F, Zeng X, Gu Y (2009) Resistance mechanism of antagonistic bacterium in plant disease biocontrol. Hubei Agric Sci 9:2286–2288

    Google Scholar 

  11. Czajkowski R, Perombelon MC, van Veen JA, van der Wolf JM (2011) Control of blackleg and tuber soft rot of potato caused by Pectobacterium and Dickeya species: a review. Plant Pathol 60:999–1013. https://doi.org/10.1111/j.1365-3059.2011.02470.x

    Article  Google Scholar 

  12. Antonia N, Teresa P (2012) Antimicrobial activity of carvacrol: current progress and future prospectives. Recent Pat Anti-Infect Drug Discov 7:28–35. https://doi.org/10.2174/157489112799829684

    Article  Google Scholar 

  13. Gutierrez-Pacheco MM, Bernal-Mercado AT, Vázquez-Armenta FJ, González-Aguilar G, Lizardi-Mendoza J, Madera-Santana T, Nazzaro F, Ayala-Zavala J (2019) Quorum sensing interruption as a tool to control virulence of plant pathogenic bacteria. Physiol Mol Plant Pathol 106:281–291. https://doi.org/10.1016/j.pmpp.2019.04.002

    Article  Google Scholar 

  14. Tapia-Rodriguez MR, Hernandez-Mendoza A, Gonzalez-Aguilar GA, Martinez-Tellez MA, Martins CM, Ayala-Zavala JF (2017) Carvacrol as potential quorum sensing inhibitor of Pseudomonas aeruginosa and biofilm production on stainless steel surfaces. Food Control 75:255–261. https://doi.org/10.1016/j.foodcont.2016.12.014

    Article  CAS  Google Scholar 

  15. Amini L, Soudi MR, Saboora A, Mobasheri H (2018) Effect of essential oil from Zataria multiflora on local strains of Xanthomonas campestris: an efficient antimicrobial agent for decontamination of seeds of Brassica oleracea var. capitata. Sci Hortic 236:256–264. https://doi.org/10.1016/j.scienta.2018.03.046

    Article  CAS  Google Scholar 

  16. Nostro A, Cellini L, Zimbalatti V, Blanco AR, Marino A, Pizzimenti F, Giulio MD, Bisignano G (2012) Enhanced activity of carvacrol against biofilm of Staphylococcus aureus and Staphylococcus epidermidis in an acidic environment. APMIS 120:967–973. https://doi.org/10.1111/j.1600-0463.2012.02928.x

    Article  CAS  PubMed  Google Scholar 

  17. Sharifi-Rad M, Varoni EM, Iriti M, Martorell M, Setzer WN, del Mar CM, Salehi B, Soltani-Nejad A, Rajabi S, Tajbakhsh M (2018) Carvacrol and human health: a comprehensive review. Phytother Res 32:1675–1687. https://doi.org/10.1002/ptr.6103

    Article  CAS  PubMed  Google Scholar 

  18. Kang J, Liu L, Liu M, Wu X, Li J (2018) 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

    Article  CAS  Google Scholar 

  19. Sánchez E, García S, Heredia N (2010) Extracts of edible and medicinal plants damage membranes of Vibrio cholerae. Appl Environ Microbiol 76:6888–6894. https://doi.org/10.1128/AEM.03052-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Shi C, Sun Y, Zheng Z, Zhang X, Song K, Jia Z, Chen Y, Yang M, Liu X, Dong R (2016) Antimicrobial activity of syringic acid against Cronobacter sakazakii and its effect on cell membrane. Food Chem 197:100–106. https://doi.org/10.1128/AEM.03052-09

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  Google Scholar 

  22. Zhang Y, Liu X, Wang Y, Jiang P, Quek S (2016) Antibacterial activity and mechanism of cinnamon essential oil against Escherichia coli and Staphylococcus aureus. Food Control 59:282–289. https://doi.org/10.1016/j.foodcont.2015.05.032

    Article  CAS  Google Scholar 

  23. 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:e0159006. https://doi.org/10.1371/journal.pone.0159006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Gutierrez-Pacheco M, Gonzalez-Aguilar G, Martinez-Tellez M, Lizardi-Mendoza J, Madera-Santana T, Bernal-Mercado A, Vazquez-Armenta F, Ayala-Zavala J (2018) Carvacrol inhibits biofilm formation and production of extracellular polymeric substances of Pectobacterium carotovorum subsp. carotovorum. Food Control 89:210–218. https://doi.org/10.1016/j.foodcont.2018.02.007

    Article  CAS  Google Scholar 

  25. Stepanovic S (2000) A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 40:175–179. https://doi.org/10.1016/S0167-7012(00)00122-6.26

    Article  CAS  PubMed  Google Scholar 

  26. Joshi JR, Burdman S, Lipsky A, Yedidia I (2015) Effects of plant antimicrobial phenolic compounds on virulence of the genus Pectobacterium. Res Microbiol 166:535–545. https://doi.org/10.1016/j.resmic.2015.04.004

    Article  CAS  PubMed  Google Scholar 

  27. Dixon RA (2001) Natural products and plant disease resistance. Nature 411:843–847. https://doi.org/10.1038/35081178

    Article  CAS  PubMed  Google Scholar 

  28. Cacciatore I, Di Giulio M, Fornasari E, Di Stefano A, Cerasa LS, Marinelli L, Turkez H, Di Campli E, Di Bartolomeo S, Robuffo I (2015) Carvacrol codrugs: a new approach in the antimicrobial plan. PLoS One 10:e0120937. https://doi.org/10.1371/journal.pone.0120937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Issam A-A, Zimmermann S, Reichling J, Wink M (2015) Pharmacological synergism of bee venom and melittin with antibiotics and plant secondary metabolites against multi-drug resistant microbial pathogens. Phytomedicine 22:245–255. https://doi.org/10.1016/j.phymed.2014.11.019

    Article  CAS  Google Scholar 

  30. Shu H, Chen H, Wang X, Hu Y, Yun Y, Zhong Q, Chen W, Chen W (2019) Antimicrobial activity and proposed action mechanism of 3-Carene against Brochothrix thermosphacta and Pseudomonas fluorescens. Molecules 24:3246. https://doi.org/10.3390/molecules24183246

    Article  CAS  PubMed Central  Google Scholar 

  31. Ultee A, Kets EPW, Smid EJ (1999) Mechanisms of action of carvacrol on the food-borne pathogen Bacillus cereus. Appl Environ Microbiol 65:4606–4610. https://doi.org/10.1089/oli.1.1999.9.487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Burt SA (2004) Essential oils: their antibacterial properties and potential applications in foods—a review. Int J Food Microbiol 94:223–253. https://doi.org/10.1016/j.ijfoodmicro.2004.03.022

    Article  CAS  PubMed  Google Scholar 

  33. Kaim G, Dimroth P (1999) ATP synthesis by F-type ATP synthase is obligatorily dependent on the transmembrane voltage. EMBO J 18:4118–4127. https://doi.org/10.1093/emboj/18.15.4118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Strahl H, Hamoen LW (2010) Membrane potential is important for bacterial cell division. Proc Natl Acad Sci USA 107:12281–12286. https://doi.org/10.1073/pnas.1005485107

    Article  PubMed  PubMed Central  Google Scholar 

  35. Stratford JP, La Edwards C, Ghanshyam MJ, Malyshev D, Delise MA, Hayashi Y, Asally M (2019) Electrically induced bacterial membrane-potential dynamics correspond to cellular proliferation capacity. Proc Natl Acad Sci USA 116:9552–9557. https://doi.org/10.1101/542746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Liu X, Cai J, Chen H, Zhong Q, Hou Y, Chen W, Chen W (2020) Antibacterial activity and mechanism of linalool against Pseudomonas aeruginosa. Microb Pathog 141:103980. https://doi.org/10.1016/j.micpath.2020.103980

    Article  CAS  PubMed  Google Scholar 

  37. Kang J, Liu L, Wu X, Sun Y, Liu Z (2018) Effect of thyme essential oil against Bacillus cereus planktonic growth and biofilm formation. Appl Microbiol Biotechnol 102:10209–10218. https://doi.org/10.1007/s00253-018-9401-y

    Article  CAS  PubMed  Google Scholar 

  38. Shen S, Zhang T, Yuan Y, Lin S, Xu J, Ye H (2015) Effects of cinnamaldehyde on Escherichia coli and Staphylococcus aureus membrane. Food Control 47:196–202. https://doi.org/10.1016/j.foodcont.2014.07.003

    Article  CAS  Google Scholar 

  39. Durand E, Lecomte J, Villeneuve P (2017) The biological and antimicrobial activities of phenolipids. Lipid Technol 29:67–70. https://doi.org/10.1002/lite.201700019

    Article  CAS  Google Scholar 

  40. Chauhan AK, Kang SC (2014) Thymol disrupts the membrane integrity of Salmonella ser. typhimurium in vitro and recovers infected macrophages from oxidative stress in an ex vivo model. Res Microbiol 165:559–565. https://doi.org/10.1016/j.resmic.2014.07.001

    Article  CAS  PubMed  Google Scholar 

  41. Inamuco J, Veenendaal AK, Burt SA, Post JA, Tjeerdsma-van Bokhoven JL, Haagsman HP, Veldhuizen EJ (2012) Sub-lethal levels of carvacrol reduce Salmonella Typhimurium motility and invasion of porcine epithelial cells. Vet Microbiol 157:200–207. https://doi.org/10.1016/j.vetmic.2011.12.021

    Article  CAS  PubMed  Google Scholar 

  42. Duan Q, Zhou M, Zhu L, Zhu G (2013) Flagella and bacterial pathogenicity. J Basic Microbiol 53:1–8. https://doi.org/10.1002/jobm.201100335

    Article  PubMed  Google Scholar 

  43. Jahn CE, Willis DK, Charkowski AO (2008) The flagellar sigma factor FliA is required for Dickeya dadantii virulence. Mol Plant Microbe Interact 21:1431–1442. https://doi.org/10.1094/MPMI-21-11-1431

    Article  CAS  PubMed  Google Scholar 

  44. Mina I, Jara N, Criollo J, Castillo J (2019) The critical role of biofilms in bacterial vascular plant pathogenesis. Plant Pathol 68:1439–1447. https://doi.org/10.1111/ppa.13073

    Article  Google Scholar 

  45. Joshi JR, Khazanov N, Senderowitz H, Burdman S, Lipsky A, Yedidia I (2016) Plant phenolic volatiles inhibit quorum sensing in pectobacteria and reduce their virulence by potential binding to ExpI and ExpR proteins. Sci Rep 6:38126. https://doi.org/10.1038/srep38126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Burt SA, Ojo-Fakunle VT, Woertman J, Veldhuizen EJ (2014) The natural antimicrobial carvacrol inhibits quorum sensing in Chromobacterium violaceum and reduces bacterial biofilm formation at sub-lethal concentrations. PLoS One 9:e93414. https://doi.org/10.1371/journal.pone.0093414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This research was supported by Grants from the Natural Science Foundation of Guangdong province (2015A030312002), the Science and Technology Project of Guangzhou city (201704030120), National Natural Science Foundation of China (31300118), Science and Technology Project of Guangdong province (2016B020202003), and the Special fund for scientific innovation strategy-construction of high level Academy of Agriculture Science (R2017PY-QY004, R2018QD-056).

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Authors and Affiliations

  1. College of Agriculture, Guangxi University, 100 Daxue Road, Nanning, 530004, China

    Shangbo Jiang, Qiqin Li & Zhongwen Wang

  2. Key Laboratory of New Techniques for Plant Protection in Guangdong, Plant Protection Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, China

    Jingxin Zhang, Qiyun Yang, Dayuan Sun, Xiaoming Pu, Huifang Shen & Birun Lin

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  1. Shangbo Jiang
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Contributions

BL conceived and designed the experiments; SJ conducted the experiments and wrote the manuscript; JZ designed the experiments and revised the paper; ZW and QL designed the experiments; DS provided materials; QY, HS, and XP analyzed the data.

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Correspondence to Zhongwen Wang or Birun Lin.

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Acknowledgements

This research was supported by Grants from the Natural Science Foundation of Guangdong province (2015A030312002), the Science and Technology Project of Guangzhou city (201704030120), National Natural Science Foundation of China (31300118), Science and Technology Project of Guangdong province (2016B020202003), and the Special fund for scientific innovation strategy-construction of high level Academy of Agriculture Science (R2017PY-QY004, R2018QD-056).

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Jiang, S., Zhang, J., Yang, Q. et al. Antimicrobial Activity of Natural Plant Compound Carvacrol Against Soft Rot Disease Agent Dickeya zeae. Curr Microbiol 78, 3453–3463 (2021). https://doi.org/10.1007/s00284-021-02609-3

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