DOI QR코드

DOI QR Code

Photoinactivation of major bacterial pathogens in aquaculture

  • Roh, Heyong Jin (Department of Aquatic life Medicine, College of Fisheries Science, Pukyong National University) ;
  • Kim, Ahran (Department of Aquatic life Medicine, College of Fisheries Science, Pukyong National University) ;
  • Kang, Gyoung Sik (Department of Aquatic life Medicine, College of Fisheries Science, Pukyong National University) ;
  • Kim, Do-Hyung (Department of Aquatic life Medicine, College of Fisheries Science, Pukyong National University)
  • 투고 : 2016.02.25
  • 심사 : 2016.08.05
  • 발행 : 2016.08.31

초록

Background: Significant increases in the bacterial resistance to various antibiotics have been found in fish farms. Non-antibiotic therapies for infectious diseases in aquaculture are needed. In recent years, light-emitting diode technology has been applied to the inactivation of pathogens, especially those affecting humans. The purpose of this study was to assess the effect of blue light (wavelengths 405 and 465 nm) on seven major bacterial pathogens that affect fish and shellfish important in aquaculture. Results: We successfully demonstrate inactivation activity of a 405/465-nm LED on selected bacterial pathogens. Although some bacteria were not fully inactivated by the 465-nm light, the 405-nm light had a bactericidal effect against all seven pathogens, indicating that blue light can be effective without the addition of a photosensitizer. Photobacterium damselae, Vibrio anguillarum, and Edwardsiella tarda were the most susceptible to the 405-nm light (36.1, 41.2, and $68.4J\;cm^{-2}$, respectively, produced one log reduction in the bacterial populations), whereas Streptococcus parauberis was the least susceptible ($153.8J\;cm^{-2}$ per one log reduction). In general, optical density (OD) values indicated that higher bacterial densities were associated with lower inactivating efficacy, with the exception of P. damselae and Vibrio harveyi. In conclusion, growth of the bacterial fish and shellfish pathogens evaluated in this study was inactivated by exposure to either the 405- or 465-nm light. In addition, inactivation was dependent on exposure time. Conclusions: This study presents that blue LED has potentially alternative therapy for treating fish and shellfish bacterial pathogens. It has great advantages in aspect of eco-friendly treating methods differed from antimicrobial methods.

키워드

참고문헌

  1. Arrojado C, Pereira C, Tome JPC, Faustino MAF, Neves MGPMS, Tome AC, Cavaleiro JAS, Cunha A, Calado R, Gomes NCM, Almeida A. Applicability of photodynamic antimicrobial chemotherapy as an alternative to inactivate fish pathogenic bacteria in aquaculture systems. Photochem Photobiol Sci. 2011;10:1691-700. https://doi.org/10.1039/c1pp05129f
  2. Ashkenazi H, Malik Z, Harth Y, Nitzan Y. Eradication of Propionibacterium acnes by its endogenic porphyrins after illumination with high intensity blue light. FEMS Immunol Med Microbiol. 2003;35:17-24. https://doi.org/10.1111/j.1574-695X.2003.tb00644.x
  3. Baeck GW, Kim JH, Gomez DK, Park SC. Isolation and characterization of Streptococcus sp. diseased flounder (Paralichthys olivaceus) in Jeju Island. J Vet Sci. 2006;7:53-8. https://doi.org/10.4142/jvs.2006.7.1.53
  4. Barnes AC, Horne MT, Ellis AE. Effect of iron on expression of superoxide dismutase by Aeromonas salmonicida and associated resistance to superoxide anion. FEMS Microbiol Lett. 1996;142:19-26. https://doi.org/10.1111/j.1574-6968.1996.tb08401.x
  5. Bostock J, McAndrew B, Richards R, Jauncey K, Telfer T, Lorenzen K, Little D, Ross L, Handisyde N, Gatward I, Corner R. Aquaculture: global status and trends. Philos T Roy Soc B. 2010;365:2897-912. https://doi.org/10.1098/rstb.2010.0170
  6. Cabello FC, Godfrey HP, Tomova A, Ivanova L, Dolz H, Millanao A, Buschmann AH. Antimicrobial use in aquaculture re-examined: its relevance to antimicrobial resistance and to animal and human health. Envrion Microbiol. 2013;15:1917-42. https://doi.org/10.1111/1462-2920.12134
  7. Dai T, Gupta A, Murray CK, Vrahas MS, Tegos GP, Hamblin MR. Blue light for infectious disease : Propionibacterium acnes, Helicobacter pylori, and beyond? Drug Resist Updat. 2012;15:223-36. https://doi.org/10.1016/j.drup.2012.07.001
  8. Dai T, Gupta A, Huang YY, Tin R, Murray CK, Vrahas MS, Sherwood ME, Tegos GT, Hamblin MR. Blue light resques mice from potentially fatal Pseudomonas aeruginosa burn infection: efficacy, safety, and mechanism of action. Antimicrob Agents Chemother. 2013;57:1238-45. https://doi.org/10.1128/AAC.01652-12
  9. Defoirdt T, Sorgeloos P, Bossier P. Alternatives to antibiotics for the control of bacterial disease in aquaculture. Curr Opin Microbiol. 2011;14:251-8. https://doi.org/10.1016/j.mib.2011.03.004
  10. Diaz-Rosales P, Chabrillon M, Arijo S, Martinez-Manzanares E, Morinigo MA, Balebona MC. Superoxide dismutase and catalase activities in Photobacterium damselae ssp. Piscicida. J Fish Dis. 2006;29:355-64. https://doi.org/10.1111/j.1365-2761.2006.00726.x
  11. Do Vale A, Ellis AE, Silva MT. Electron microscopic evidence that expression of capsular polysaccarhide by Photobacterium damselae subsp. piscicida is dependent on iron availability and growth phase. Dis Aquat Organ. 2001;44:237-40. https://doi.org/10.3354/dao044237
  12. Flint DH, Tuminello JF, Emptage MH. The inactivation of Fe-S cluster containing hydrolases by superoxide. J Biol Chem. 1993;268:22369-76.
  13. Ghanizadeh KE, Khodabandeh S. Effects of ultraviolet radiation on skin structure and ultrastructure in Caspian Sea salmon, Salmo trutta caspius, during alevin stage. Toxicol Environ Chem. 2010;92:903-14. https://doi.org/10.1080/02772240903127284
  14. Guardabassi L, Dalsgaard A, Raffatellu M, Olsen JE. Increase in the prevalence of oxolinic acid resistant Acinetobacter spp. Observed in a stream receiving the effluent from a freshwater trout farm following the treatment with oxolinic acid-medicated feed. Aquaculture. 2000;188:205-18. https://doi.org/10.1016/S0044-8486(00)00340-9
  15. Hamblin MR, Viveiros J, Yang C, Ahmadi A, Ganz RA, Tolkoff MJ. Helicobacter pylori accumulates photoactive porphyrins and is killed by visible light. Antimicrob Agents Chemother. 2005;4:2822-7.
  16. Han HJ, Kim DH, Lee DC, Kim SM, Park SI. Pathogenicity of Edwardsiella tarda to olive flounder, Paralichthys olivaceus. J Fish Dis. 2006;29:601-9. https://doi.org/10.1111/j.1365-2761.2006.00754.x
  17. Han HJ, Kim DY, Kim WS, Kim CS, Jung SJ, Oh MJ, Kim DH. Atypical Aeromonas salmonicida infection in the black rockfish, sebastes schlegeli Hilgendorf, in Korea. J Fish Dis. 2011;34:47-55. https://doi.org/10.1111/j.1365-2761.2010.01217.x
  18. Jori G, Fabris C, Soncin M, Ferro S, Coppellotti O, Dei D, Fantetti L, Chiti G, Roncucci G. Photodynamic therapy in the treatment of microbial infections: basic principles and perspective applications. Laser Surg Med. 2006;38:468-81. https://doi.org/10.1002/lsm.20361
  19. Kaweewat K, Hofer R. Effect of UV-B radiation on goblet cells in the skin of different fish species. J Photochem Photobiol B. 1997;41:222-6. https://doi.org/10.1016/S1011-1344(97)00104-8
  20. Kleinpenning MM, Smits T, Frunt MHA, Van Erp PEJ, Van de Kerkhof PCM, Gerritsen RMJP. Clinical and histological effects of blue light on normal skin. Photodermatol Photo. 2010;26:16-21. https://doi.org/10.1111/j.1600-0781.2009.00474.x
  21. Lipovsky A, Nitzan Y, Gedanken A, Lubart R. Visible light-induced killing of bacteria as a function of wavelength: implication for wound healing. Laser Surg Med. 2010;42:467-72. https://doi.org/10.1002/lsm.20948
  22. Maclean M, Macgregor SJ, Anderson JG, Woolsey G. The role of oxygen in the visible-light inactivation of Staphylococcus aureus. J Photochem Photobiol B. 2008;92:180-4. https://doi.org/10.1016/j.jphotobiol.2008.06.006
  23. Maclean M, Macgregor SJ, Anderson JG, Woolsey G. Inactivation of bacterial pathogens following exposure to light from a 405-nanometer light-emitting diode array. Appl Environ Microbiol. 2009;75:1932-7. https://doi.org/10.1128/AEM.01892-08
  24. Maclean M, MacGregor SJ, Anderson JG, Woolsey GA, Coia JE, Hamilton K, Taggart I, Watson SB, Thakker B, Gettinby G. Environmental decontamination of a hospital isolation room using high-intensity narrow-spectrum light. J Hosp Infect. 2010;76:247-51. https://doi.org/10.1016/j.jhin.2010.07.010
  25. Maisch T. A new strategy to destroy antibiotic resistant microorganisms: antimicrobial photodynamic treatment. Mini-Rev Med Chem. 2009;9:974-83. https://doi.org/10.2174/138955709788681582
  26. Mata AI, Gibello A, Casamayor A, Blanco MM, Dominguez L, Fernandez-Garayzabal JF. Multiplex PCR assay for detection of bacterial pathogens associated with warmwater streptococcosis in fish. Appl Environ Microbiol. 2004;70:3183-7. https://doi.org/10.1128/AEM.70.5.3183-3187.2004
  27. Migaud H, Cowan M, Taylor J, Ferguson HW. The effect of spectral composition and light intensity on melatonin, stress and retinal damage in post-smolt Atlantic salmon, Salmo salar. Aquaculture. 2007;270:390-404. https://doi.org/10.1016/j.aquaculture.2007.04.064
  28. Milton DL, Toole RO', Horstedt P, Wolf-Watz H. Flagellin A is essential for the virulence of Vibrio anguillarium. J Bacteriol. 1996;178:1310-9. https://doi.org/10.1128/jb.178.5.1310-1319.1996
  29. Murdoch LE, Maclean M, Endarko E, MacGregor SJ, Anderson JG. Bactericidal effects of 405 nm light exposure demonstrated by inactivation of Escherichia, Salmonella, Shigella, Listeria, and Mycobacterium species in liquid suspensions and on exposed surfaces. Sci World J. 2012;2012:1-8.
  30. Naka H, Hirono I, Aoki T. Molecular cloning and functional analysis of Photobacterium damselae subsp. piscicida heme receptor gene. J Fish Dis. 2005;28:81-8. https://doi.org/10.1111/j.1365-2761.2004.00601.x
  31. Osorio CR, Toranzo AE, Romalde JL, Barja JL. Multiplex PCR assay for ureC and 16S rRNA genes clearly discriminates between both subspecies of Photobacterium damselae. Dis Aquat Organ. 2000;40:177-83. https://doi.org/10.3354/dao040177
  32. Pang L, Zhang XH, Zhong Y, Chen J, Li Y, Austin B. Identification of Vibrio haveyi using PCR amplification of the ToxR gene. Lett Appl Microbiol. 2006;43:249-55. https://doi.org/10.1111/j.1472-765X.2006.01962.x
  33. Pridgeon JW, Klesius PH. Major bacterial diseases in aquaculture and their vaccine development. In: Hemming D, editor. Anim Sci Rev 2012. UK: CAB International; 2013. p. 141-56.
  34. Romalde JL. Photobacterium damselae subsp. Piscicida: an integrated view of a bacterial fish pathogen. Int Microbiol. 2002;5:3-9. https://doi.org/10.1007/s10123-002-0051-6
  35. Schmidt AS, Bruun MS, Dalsgaard I, Pedersen K, Larsen JL. Occurrence of antimicrobial resistance in fish-pathogenic and environmental bacteria associated with four Danish rainbow trout farms. Appl Environ Microbiol. 2000;66:4908-15. https://doi.org/10.1128/AEM.66.11.4908-4915.2000
  36. Subasinghe RP, Bondad-Reantaso MG, McGladdery SE. Aquaculture development, health and wealth. In: Subasinghe RP, Bueno P, Phillips MJ, Hough C, McGladdery SE, Arthur JR, editors. In proceedings of the Conference on Aquaculture in the Third Millennium: 20-25 February 2000. Bangkok: NACA and FAO; 2001. p. 167-91.
  37. Vattanaviboon P, Mongkolsuk S. Unusual adaptive, cross protection responses and growth phase resistance against peroxide killing in a bacterial shrimp pathogen. Vibrio harveyi. FEMS Microbiol Lett. 2001;200:111-6. https://doi.org/10.1111/j.1574-6968.2001.tb10701.x
  38. Villamizar N, Blanco-Vives N, Migaud H, Davie A, Carboni S, Sanchez-Vazquez FJ. Effects of light during early larval development of some aquacultured teleosts: a review. Aquaculture. 2011;315:86-94. https://doi.org/10.1016/j.aquaculture.2010.10.036
  39. Weinstein MR, Litt M, Kertesz DA, Wyper P, Rose D, Coulter M, McGeer A, Facklam R, Ostach C. Invasive infections due to a fish pathogen, Streptococcus iniae. New Engl J Med. 1997;28:589-94.
  40. Wiklund T, Dalsgaard I. Occurrence and significance of atypical Aeromonas salmonicida in non-salmonid and salmoid fish species. Dis Aquat Organ. 1998;32:49-69. https://doi.org/10.3354/dao032049
  41. Won KM, Park SI. Pathogenicity of Vibrio harveyi to culture marine fishes in Korea. Aquaculture. 2008;285:8-13. https://doi.org/10.1016/j.aquaculture.2008.08.013
  42. Yesilkaya H, Kadioglu A, Gingles N, Alexander JE, Mitchell TJ, Andrew PW. Role of manganese-containing superoxide dismutase in oxidative stress and virulence of Streptococcus pneumoniae. Infect Immun. 2000;68:2819-26. https://doi.org/10.1128/IAI.68.5.2819-2826.2000
  43. Yin Y, Gupta A, Hamblin MR. Light based anti-infectives: ultraviolet C irradiation, photodynamic therapy, blue light, and beyond. Curr Opin Pharmacol. 2013;13:731-62. https://doi.org/10.1016/j.coph.2013.08.009

피인용 문헌

  1. Antimicrobial blue light inactivation of pathogenic microbes: State of the art vol.33, pp.None, 2016, https://doi.org/10.1016/j.drup.2017.10.002
  2. Antimicrobial Blue Light versus Pathogenic Bacteria: Mechanism, Application in the Food Industry, Hurdle Technologies and Potential Resistance vol.9, pp.12, 2020, https://doi.org/10.3390/foods9121895
  3. Genotypic and Phenotypic Characterization of Highly Alkaline-Resistant Carnobacterium maltaromaticum V-Type ATPase from the Dairy Product Based on Comparative Genomics vol.9, pp.6, 2021, https://doi.org/10.3390/microorganisms9061233