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Food Science and Biotechnology

, Volume 26, Issue 6, pp 1649–1657 | Cite as

Characterization and evaluation of antimicrobial activity of actinonin against foodborne pathogens

  • Dongyun Jung
  • Su-Jin Yum
  • Hee Gon JeongEmail author
Article

Abstract

This study revealed the antimicrobial properties of actinonin against major foodborne pathogens, Escherichia coli O157:H7, Listeria monocytogenes, Salmonella Typhimurium, Staphylococcus aureus, and Vibrio vulnificus. Among them, actinonin caused growth defect in S. Typhimurium and V. vulnificus. Minimal inhibitory concentration (MIC) values of actinonin were determined by broth microdilution methods. The MICs of actinonin were ≤0.768 μg/ml for S. Typhimurium and ≤0.192 μg/ml for V. vulnificus. Susceptibility to actinonin in both pathogens was measured by colony-forming ability and disc diffusion test. The results showed actinonin had antimicrobial activity against S. Typhimurium and V. vulnificus in a dose-dependent manner. The inhibitory effects on swarming motility were determined, and cytotoxicity of each pathogen against HeLa cells was decreased significantly by actinonin treatment. Furthermore, actinonin showed an antimicrobial efficacy in food models infected with these pathogens. These results demonstrate that actinonin is potentially an effective agent for food sanitization or preservation.

Keywords

Actinonin Foodborne pathogens Antimicrobial agent 

Notes

Acknowledgements

This work was supported by a Grant from the National Research Foundation of Korea funded by the Korean Government (NRF-2014R1A1A1002580) and the Ministry of Food and Drug Safety, Republic of Korea (14162MFDS972).

Compliance with ethical standards

Conflicts of interest

The authors declare no conflict of interest.

References

  1. 1.
    Newell DG, Koopmans M, Verhoef L, Duizer E, Aidara-Kane A, Sprong H, Opsteegh M, Langelaar M, Threfall J, Scheutz F, van der Giessen J, Kruse H. Food-borne diseases—The challenges of 20 years ago still persist while new ones continue to emerge. Int J. Food Microbiol. 139: S3–S15 (2010)CrossRefGoogle Scholar
  2. 2.
    Wimley WC, Hristova K. Antimicrobial peptides: successes, challenges and unanswered questions. The J. Membrane Biol. 239: 27–34 (2011)CrossRefGoogle Scholar
  3. 3.
    Bashiardes G, Bodwell GJ, Davies SG. Asymmetric synthesis of (-)-Actinonin and (-)-epi-actinonin. J. Chem. Soc. Perkin Trans. 1: 459–469 (1993)CrossRefGoogle Scholar
  4. 4.
    Lee MD, She YH, Soskis MJ, Borella CP, Gardner JR, Hayes PA, Dy BM, Heaney ML, Philips MR, Bornmann WG, Sirotnak FM, Scheinberg DA. Human mitochondrial peptide deformylase, a new anticancer target of actinonin-based antibiotics. J. Clin. Invest. 114: 1107–1116 (2004)CrossRefGoogle Scholar
  5. 5.
    Chen DZ, Patel DV, Hackbarth CJ, Wang W, Dreyer G, Young DC, Margolis PS, Wu C, Ni ZJ, Trias J, White RJ, Yuan ZY. Actinonin, a naturally occurring antibacterial agent, is a potent deformylase inhibitor. Biochemistry 39: 1256–1262 (2000)CrossRefGoogle Scholar
  6. 6.
    Yang N, Sun C. The inhibition and resistance mechanisms of actinonin, isolated from marine Streptomyces sp. NHF165, against Vibrio anguillarum. Frontiers in Microbiol. 7: 1467 (2016)Google Scholar
  7. 7.
    Duroc Y, Giglione C, Meinnel T. Mutations in three distinct loci cause resistance to peptide deformylase inhibitors in Bacillus subtilis. Antimicrob. Agents and Chemother. 53: 1673–1678 (2009)CrossRefGoogle Scholar
  8. 8.
    Margolis P, Hackbarth C, Lopez S, Maniar M, Wang W, Yuan Z, White R, Trias J. Resistance of Streptococcus pneumoniaeto Deformylase Inhibitors Is Due to Mutations indefB. Antimicrob. Agents and Chemother. 45: 2432–2435 (2001)CrossRefGoogle Scholar
  9. 9.
    Wiegand I, Hilpert K, Hancock RE. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Prot. 3: 163–175 (2008)CrossRefGoogle Scholar
  10. 10.
    Patel J, Cockerill F, Alder J, Bradford P, Eliopoulos G, Hardy D. Performance standards for antimicrobial susceptibility testing; twenty-fourth informational supplement. CLSI Stand. Antimicrob. Suscept. Testing 34: 1–226 (2014)Google Scholar
  11. 11.
    Na HS, Cha MH, Oh DR, Cho CW, Rhee JH, Kim YR. Protective mechanism of curcumin against Vibrio vulnificus infection. Fems Immunol. Med. Microbiol. 63: 355–362 (2011)CrossRefGoogle Scholar
  12. 12.
    Park KS, Ono T, Rokuda M, Jang MH, Okada K, Idia T, Honda T. Functional characterization of two type III secretion systems of Vibrio parahaemolyticus. Infect. Immun. 72: 6659–6665 (2004)CrossRefGoogle Scholar
  13. 13.
    Wang Y, Lu ZX, Wu H, Lv FX. Study on the antibiotic activity of microcapsule curcumin against foodborne pathogens. Int. J. Food Microbiol. 136: 71–74 (2009)CrossRefGoogle Scholar
  14. 14.
    Menousek J, Mishra B, Hanke ML, Heim CE, Kielian T, Wang G. Database screening and in vivo efficacy of antimicrobial peptides against methicillin-resistant Staphylococcus aureus USA300. Int. J. Antimicrob. Agents 39: 402–406 (2012)CrossRefGoogle Scholar
  15. 15.
    Montesinos E. Antimicrobial peptides and plant disease control. FEMS Microbiol. Lett. 270: 1–11 (2007)CrossRefGoogle Scholar
  16. 16.
    Hancock RE, Chapple DS. Peptide antibiotics. Antimicrob. agents and chemother. 43: 1317–1323 (1999)Google Scholar
  17. 17.
    Margolis PS, Hackbarth CJ, Young DC, Wang W, Chen D, Yuan ZY, White R, Trias J. Peptide deformylase in Staphylococcus aureus: Resistance to inhibition is mediated by mutations in the formyltransferase gene. Antimicrob. Agents and Chemother. 44: 1825–1831 (2000)CrossRefGoogle Scholar
  18. 18.
    Mcmurry LM, Oethinger M, Levy SB. Overexpression of marA, soxS, or acrAB produces resistance to triclosan in laboratory and clinical strains of Escherichia coli. FEMS Microbiol. Lett. 166: 305–309 (1998)CrossRefGoogle Scholar
  19. 19.
    Romanova NA, Wolffs PFG, Brovko LY, Griffiths MW. Role of efflux pumps in adaptation and resistance of Listeria monocytogenes to benzalkonium chloride. Appl. Environ. Microbiol. 72: 3498–3503 (2006)CrossRefGoogle Scholar
  20. 20.
    Stavri M, Piddock LJV, Gibbons S. Bacterial efflux pump inhibitors from natural sources. J. Antimicrob. Chemother. 59: 1247–1260 (2007)CrossRefGoogle Scholar
  21. 21.
    Gyawali R, Ibrahim SA. Natural products as antimicrobial agents. Food Contr. 46: 412–429 (2014)CrossRefGoogle Scholar
  22. 22.
    Liu Y, Han F, Xie Y, Wang Y. Comparative antimicrobial activity and mechanism of action of bovine lactoferricin-derived synthetic peptides. Biometals 24: 1069–1078 (2011)CrossRefGoogle Scholar
  23. 23.
    Gill AO, Holley RA. Interactive inhibition of meat spoilage and pathogenic bacteria by lysozyme, nisin and EDTA in the presence of nitrite and sodium chloride at 24 C. Int. J. Food Microbiol. 80: 251–259 (2003)CrossRefGoogle Scholar
  24. 24.
    Palaniappan K, Holley RA. Use of natural antimicrobials to increase antibiotic susceptibility of drug resistant bacteria. Int. J. Food Microbiol. 140: 164–168 (2010)CrossRefGoogle Scholar
  25. 25.
    de Castro RD, de Souza TM, Bezerra LM, Ferreira GL, de Brito Costa EM, Cavalcanti AL. Antifungal activity and mode of action of thymol and its synergism with nystatin against Candida species involved with infections in the oral cavity: an in vitro study. BMC Complementary and Altern. Med. 15: 417 (2015)CrossRefGoogle Scholar
  26. 26.
    Sang Y, Ortega MT, Rune K, Xiau W, Zhang G, Soulages JL, Lushington GH, Fang J, Williams TD, Blecha F. Canine cathelicidin (K9CATH): gene cloning, expression, and biochemical activity of a novel pro-myeloid antimicrobial peptide. Dev. Comp. Immunol. 31: 1278–1296 (2007)CrossRefGoogle Scholar
  27. 27.
    Trinh N-T-T, Dumas E, Thanh ML, Degraeve P, Amara CB, Gharsallaoui A, Oulahal N. Effect of a Vietnamese Cinnamomum cassia essential oil and its major component trans-cinnamaldehyde on the cell viability, membrane integrity, membrane fluidity, and proton motive force of Listeria innocua. Canadian J. Microbiol. 61: 263–271 (2015)CrossRefGoogle Scholar
  28. 28.
    Packiavathy I, Sasikumar P, Pandian S, Veera Ravi A. Prevention of quorum-sensing-mediated biofilm development and virulence factors production in Vibrio spp. by curcumin. Appl. Microbiol. Biotechnol. 97: 10177–10187 (2013)CrossRefGoogle Scholar
  29. 29.
    Dorrington T, Gomez-Chiarri M. Antimicrobial peptides for use in oyster aquaculture: effect on pathogens, commensals, and eukaryotic expression systems. J. Shellfish Res. 27: 365–373 (2008)CrossRefGoogle Scholar
  30. 30.
    Yin M, Liu D, Xu F, Xiao L, Wang Q, Wang B, Chang Y, Zheng J, Tao X, Liu G. A specific antimicrobial protein CAP-1 from Pseudomonas sp. isolated from the jellyfish Cyanea capillata. Int. J. Biologic. Macromol. 82: 488–496 (2016)CrossRefGoogle Scholar
  31. 31.
    Arumugam M, Mitra A, Jaisankar P, Dasgupta S, Sen T, Gachhui R, Mukhopadhyay UK, Mukherjee J. Isolation of an unusual metabolite 2-allyloxyphenol from a marine actinobacterium, its biological activities and applications. Appl. Microbiol. Biotechnol. 86: 109–117 (2010)CrossRefGoogle Scholar
  32. 32.
    Kearns DB. A field guide to bacterial swarming motility. Nature Rev. Microbiol. 8: 634–644 (2010)CrossRefGoogle Scholar
  33. 33.
    Lhocine N, Arena ET, Bomme P, Ubelmann F, Prévost M-C, Robine S, Sansonetti PJ. Apical invasion of intestinal epithelial cells by Salmonella typhimurium requires villin to remodel the brush border actin cytoskeleton. Cell host microbe 17: 164–177 (2015)CrossRefGoogle Scholar
  34. 34.
    Jeong H-G, Satchell KJ. Additive function of Vibrio vulnificus MARTX Vv and VvhA cytolysins promotes rapid growth and epithelial tissue necrosis during intestinal infection. PLoS Pathog 8: e1002581 (2012)CrossRefGoogle Scholar
  35. 35.
    Glass KA, Johnson EA. Antagonistic effect of fat on the antibotulinal activity of food preservatives and fatty acids. Food Microbiol. 21: 675–682 (2004)CrossRefGoogle Scholar

Copyright information

© The Korean Society of Food Science and Technology and Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.Department of Food Science and Technology, College of Agriculture and Life SciencesChungnam National UniversityYuseong-GuSouth Korea

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