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Distribution of resistance genes against lincomycin of pathogenic bacteria isolated from cultured olive flounder (Paralichthys olivaceus)

양식 넙치에서 분리한 어병세균의 lincomycin에 대한 내성 유전자의 분포

  • Kim, Ye Ji (Department of Marine Life Sciences, Jeju National University) ;
  • Jun, Lyu Jin (Department of Marine Life Sciences, Jeju National University) ;
  • Lee, Young Juhn (Department of Marine Life Sciences, Jeju National University) ;
  • Ko, Ye Jin (Department of Marine Life Sciences, Jeju National University) ;
  • Han, So Ri (Fishcare laboratory) ;
  • Kim, Sung Hyun (Fishcare laboratory) ;
  • Jeong, Joon Bum (Department of Marine Life Sciences, Jeju National University)
  • 김예지 (제주대학교 해양생명과학과) ;
  • 전려진 (제주대학교 해양생명과학과) ;
  • 이영준 (제주대학교 해양생명과학과) ;
  • 고예진 (제주대학교 해양생명과학과) ;
  • 한소리 (피쉬케어연구소) ;
  • 김성현 (피쉬케어연구소) ;
  • 정준범 (제주대학교 해양생명과학과)
  • Received : 2022.04.29
  • Accepted : 2022.05.27
  • Published : 2022.06.30

Abstract

Lincomycin as one of the lincosamides antibiotics have been mainly used in human and livestock fields, but have not been used in aquaculture. In this study, the distribution of minimum inhibitory concentration (MIC) values against lincomycin and the detection of the macrolide-lincosamide-streptogramin (MLS) resistance gene were confirmed in bacterial pathogens isolated from cultured olive flounder (Paralichthys olivaceus). Of the 107 strains isolated from Jeju, 36 strains of Gram-positive bacteria and 71 strains of Gram-negative bacteria were identified. Most of Streptococcus spp. was found to have a MIC value of less than or equal to 0.5 ㎍/mL, and Edwardsiella piscicida was found to have a MIC value higher than 1,024 ㎍/mL. V. harveyi and V. alginolyticus mostly showed MIC values of 256 ㎍/mL, but V. scophthalmi displayed values of 8~64 ㎍/mL. In the detection of MLS resistance gene, erm(B) was detected in 9 strains of Streptococcus spp., and erm(A) was confirmed in one strain.

Keywords

Acknowledgement

이 논문은 2021학년도 제주대학교 교원성과지원사업에 의하여 연구되었음.

References

  1. Achard, A., Guerin-Faublee, V., Pichereau, V., Villers, C. and Leclercq, R.: Emergence of macrolide resistance gene mph(B) in Streptococcus uberis and cooperative effects with rdmC-Like gene. Animicrob. Agents Chemother., 52:2767-2770, 2008. https://doi.org/10.1128/AAC.00481-08
  2. Bozdogan, B., Berrezouga, L., Kuo, M.S., Yurek, D.A., Farley, K.A., Stockman, B.J. and Leclercq, R.: A new resistance gene, linB, conferring resistance to lincosamides by nucleotidylation in Enterococcus faecium HM1025. Animicrob. Agents Chemother., 43:925-929, 1999. https://doi.org/10.1128/AAC.43.4.925
  3. Chen, Y.M., Holmes, E.C., Chen, X., Tian, J.H., Lin, X.D., Qin, X.C., Gao, W.H., Liu, J., Wu, Z.D. and Zhang, Y.Z.: Diverse and abundant resistome in terrestrial and aquatic vertebrates revealed by transcriptional analysis. Sci. Rep., 10:18870, 2020. https://doi.org/10.1038/s41598-020-75904-x
  4. Cho, Y.R., Kim, H.S., Kim, S.K., Kim, S.R., Hur, Y.B. and Kim, J.H.: Bio-floc technology application in olive flounder, Paralichthys olivaceus aquaculture according to the difference of closed recirculating systems. Korean J. Environ. Biol., 37:129-135, 2019. https://doi.org/10.11626/KJEB.2019.37.2.129
  5. Chung, W.O., Werckenthin, C., Schwarz, S. and Roberts, M.C.: Host range of the ermF rRNA methylase gene in bacteria of human and animal origin. J. Antimicrob. Chemother., 43:5-14, 1999. https://doi.org/10.1093/jac/43.1.5
  6. Griffin, M.J., Ware, C., Quiniou, S.M., Steadman, J.M., Gaunt, P.S., Khoo, L.S. and Soto, E.: Edwardsiella piscicida identified in the southeastern USA by gyrB sequence, species-specific and repetitive sequence-mediated PCR. Dis. Aquat. Org., 108:23-35, 2014. https://doi.org/10.3354/dao02687
  7. Haenni, M., Saras, E., Chaussiere, S., Treilles, M. and Madec, J.Y.: ermB-mediated erythromycin resistance in Streptococcus uberis from bovine mastitis. Vet. J., 189:356-358, 2011. https://doi.org/10.1016/j.tvjl.2010.06.021
  8. Hammerum, A.M., Jensen, L.B. and Aarestrup, F.M.: Detection of the satA gene and transferability of virginiamycin resistance in Enterococcus faecium from food-animals. FEMS Microbiol. Lett, 168:145-151, 1998. https://doi.org/10.1016/S0378-1097(98)00433-9
  9. Hung, S.W., Wang, S.L., Tu, C.Y., Tsai, Y.C., Chuang, S.T., Shieh, M.T., Liu, P.C. and Wang, W.S.: Antibiotic susceptibility and prevalence of erythromycin ribosomal methylase gene, erm(B) in Streptococcus spp.. Vet. J., 176:197-204, 2008. https://doi.org/10.1016/j.tvjl.2007.02.008
  10. Hwang, S.D., Jo, D.H., Cho, M.Y., Jee, B.Y., Park, M.A. and Park, C.I.: Application of water-soluble tetrazolium salt for development of rapid antimicrobial susceptibility testing methods. J. Fish. Pathol, 28:71-78, 2015. https://doi.org/10.7847/JFP.2015.28.2.071
  11. Jang, H.M., Kim, Y.B., Choi, S.K., Lee, Y.H., Shin, S.G., Unno, T. and Kim, Y.M.: Prevalence of antibiotic resistance genes from effluent of coastal aquaculture, South Korea. Environ. Pollut., 233:1049-1057, 2018. https://doi.org/10.1016/j.envpol.2017.10.006
  12. Jee, B.Y., Min, J.G., Kim, T.J., Choi, J.S. and Park, S. M.: Research on sanitation control for an HACCP application for a flatfish (Paralichthys olivaceus) aquaculture farm. J. Fish Mar. Sci. Edu., 25:1179-1191, 2013. https://doi.org/10.13000/JFMSE.2013.25.5.1179
  13. Jung, Y.H., Shin, E.S., Kim, O., Yoo, J.S., Lee, K.M., Yoo, J.I., Chung, G.T. and Lee, Y.S.: Characterization of two newly identified genes, vgaD and vatG, conferring resistance to streptogramin a in Enterococcus faecium. Animicrob. Agents Chemother., 54:4744-4749, 2010. https://doi.org/10.1128/AAC.00798-09
  14. Kim, B.Y., Jeon, J.H., Choi, S.K., Shin, J.G., Lee, Y.H. and Kim, Y.M.: Use of a filtering process to remove solid waste and antibiotic resistance genes from effluent of a flow-through fish farm. Sci. Total Environ., 615:289-296, 2018. https://doi.org/10.1016/j.scitotenv.2017.09.279
  15. Kim, H.J., Ryu, J.O., Lee, S.Y., Kim, E.S. and Kim, H.Y.: Multiplex PCR for detection of the Vibrio genus and five pathogenic Vibrio species with primer sets designed using comparative genomics. BMC Microbiol., 15:239, 2015. https://doi.org/10.1186/s12866-015-0577-3
  16. Kim, H.Y., Lee I.S. and Oh, J.E.: Human and veterinary pharmaceuticals in the marine environment including fish farms in Korea. Sci. Total Environ., 579:940-949, 2017. https://doi.org/10.1016/j.scitotenv.2016.10.039
  17. Kim, M.S., Cho, J.Y. and Choi, H.S.: Identification of Vibrio harveyi, Vibrio ichthyoenteri, and Photobacterium damselae isolated from olive flounder Paralichthys olivaceus in Korea by multiplex PCR developed using the rpoB gene. Fish Sci., 80:333-339, 2014. https://doi.org/10.1007/s12562-014-0702-5
  18. Korean Statistical Information Service (KOSIS). Retrieved from http://kosis.kr. 2022.
  19. Kwon, M.G., Lim, Y.J., Kim, M.S., Seo J.S. and Kim, D.H.: Epidemiological cut-off values generated for disc diffusion data from Photobacterium damselae. J. Fish Aquat. Sci., 49:838-844, 2016.
  20. Landoni, M.F. and Albarellos, G.: The use of antimicrobial agents in broiler chickens. Vet. J., 205:21-27, 2015. https://doi.org/10.1016/j.tvjl.2015.04.016
  21. Leclercq, R.: Mechanisms of resistance to macrolides and lincosamides: Nature of the resistance elements and their clinical implications. Clin. Infect. Dis., 34:482-492, 2002. https://doi.org/10.1086/324626
  22. Lee, S.H., Jung, H.W., Jung, J.Y., Min, H.J., Kim, B.R., Park, C.G., Oh, J.E., Onoda, Y. and Satou, N.: Characteristics of occurrence of pharmaceuticals in the Nakdong river. J. Kor. Soc. Environ. Eng., 35:45-56, 2013. https://doi.org/10.4491/KSEE.2013.35.1.045
  23. Li, L., Sun, J., Liu, B., Zhao, D., Ma, J., Deng, H., Li, X., Hu, F., Liao, X. and Liu, Y.: Quantification of lincomycin resistance genes associated with lincomycin residues in waters and soils adjacent to representative swine farms in China. Front. Microbiol., 4:364, 2013. https://doi.org/10.3389/fmicb.2013.00364
  24. Li, Y., Fu, L., Li, X., Wang, Y., Wei, Y., Tang, J. and Liu, H.: Novel strains with superior degrading efficiency for lincomycin manufacturing biowaste. Ecotoxicol. Environ. Saf., 209:111802, 2021. https://doi.org/10.1016/j.ecoenv.2020.111802
  25. Lina, G., Quaglia, A., Reverdy, M.E., Leclercq, R., Vandenesch, F. and Etienne, J.: Distribution of genes encoding resistance to macrolides, lincosamides, and streptogramins among Staphylococci. Antimicrob. Agents Chemother., 43:1062-1066, 1999. https://doi.org/10.1128/aac.43.5.1062
  26. Luna, V.A., Cousin, S., JR, Whittington, W.L. and Roberts, M.C.: Identification of the conjugative mef gene in clinical Acinetobacter junii and Neisseria gonorrhoeae isolates. Animicrob. Agents Chemother., 44:2503-2506, 2000. https://doi.org/10.1128/AAC.44.9.2503-2506.2000
  27. Maes, D., Boyen, F., Haesebrouck, F. and Gautier-Bouchardon, A.V.: Antimicrobial treatment of Mycoplasma hyopneumoniae infections. Vet. J., 259:105474, 2020.
  28. Mehrtens, A., Licha, T. and Burke, V.: Occurrence, effects and behaviour of the antibiotic lincomycin in the agricultural and aquatic environment - A review. Sci. Total Environ., 778:146306, 2021. https://doi.org/10.1016/j.scitotenv.2021.146306
  29. Ministry of Agriculture, Food and Rural Affairs, National antibiotic use and resistance monitoring-Animals, livestock and marine products. Retrieved from https://www.qia.go.kr/viewwebQiaCom.do?id=53852&type=50_1ndyjsy. 2020.
  30. National Institute of Fisheries Science (NIFS). Retrieved from https://www.nifs.go.kr/page?id=antibiotics_1_08. 2022.
  31. Nonaka, L., Maruyama, F., Suzuki, S. and Masuda, M.: Novel macrolide-resistance genes, mef(C) and mph (G), carried by plasmids from Vibrio and Photobacterium isolated from sediment and seawater of a coastal aquaculture site. Lett. Appl. Microbiol., 61:1-6, 2015. https://doi.org/10.1111/lam.12414
  32. Normark, B.H. and Normark, S.: Evolution and spread of antibiotic resistance. J. Intern. Med., 252:91-106, 2002. https://doi.org/10.1046/j.1365-2796.2002.01026.x
  33. Park, Y.K., Nho, S.W., Shin, G.W., Park, S.B., Jang, H.B., Cha, I.S., Ha, M.A., Kim, Y.R., Dalvi, R.S., Kang, B.J. and Jung, T.S.: Antibiotic susceptibility and resistance of Streptococcus iniae and Streptococcus parauberis isolated from olive flounder (Paralichthys olivaceus). Vet. Microbiol., 136:76-81, 2009. https://doi.org/10.1016/j.vetmic.2008.10.002
  34. Pepi, M. and Focardi, S.: Antibiotic-resistant bacteria in aquaculture and climate change: A challenge for health in the mediterranean area. Int. J. Environ. Res. Public Health, 18:5723, 2021. https://doi.org/10.3390/ijerph18115723
  35. Roberts, M.C., Sutcliffe, J., Courvalin, P., Jensen, L.B., Rood, J. and Seppala, H.: Nomenclature for macrolide and macrolide-lincosamide-streptogramin B resistance determinants. Antimicrob. Agents Chemother., 43:2823-2830, 1999. https://doi.org/10.1128/aac.43.12.2823
  36. Roberts, M.C.: Distribution of macrolide, lincosamide, streptogramin, ketolide and oxazolidinone (MLSKO) resistance genes in gram-negative bacteria. Curr. Drug Targets Infect. Disord., 4:207-215, 2004. https://doi.org/10.2174/1568005043340678
  37. Roberts, M.C.: Environmental macrolide-lincosamide-streptogramin and tetracycline resistant bacteria. Front. Microbiol., 2: 40, 2011. https://doi.org/10.3389/fmicb.2011.00040
  38. Saenz, J.S., Marques, T.V., Barone, R.S.C., Cyrino, J.E.P., Kublik, S., Nesme, J., Schloter, M., Rath, S. and Vestergaard, G.: Oral administration of antibiotics increased the potential mobility of bacterial resistance genes in the gut of the fish Piaractus mesopotamicus. Microbiome, 7:24, 2019. https://doi.org/10.1186/s40168-019-0632-7
  39. Seo, J.S., Jeon, E.J., Kwon, M.G., Hwang, J.Y., Jung, S.H., Kim, N.Y., Jee, B.Y. and Park, M.A.: Disease resistance against bacterial infection on treatment of hot-water extract with 6 herbal mixtures in olive flounder Paralichthys olivaceus. J. Fish Mar. Sci. Edu., 28:1715-1723, 2016. https://doi.org/10.13000/JFMSE.2016.28.6.1715
  40. Societe Francaise de Microbiologie. Comite de l'Antibiogramme de la Societe Francaise de Microbiologie (CA-SFM) Recommandations Veterinaires. 2019.
  41. Spizek, J. and Rezanka, T.: Lincomycin, clindamycin and their applications. Appl. Microbiol. Biotechnol., 64:455-464, 2004. https://doi.org/10.1007/s00253-003-1545-7
  42. Sutcliffe, J., Grebe, T., Tait-Kamradt, A. and Wondrack, L.: Detection of erythromycin-resistant determinants by PCR. Animicrob. Agents Chemother., 40:2562-2566, 1996. https://doi.org/10.1128/AAC.40.11.2562
  43. Tenover, F.C.: Mechanisms of antimicrobial resistance in bacteria. Am. J. Med., 34:S3-S10, 2006. https://doi.org/10.1016/j.amjmed.2006.03.011
  44. Thiang, E.L., Lee, C.W., Takada, H., Seki, K., Takei, A., Suzuki, S., Wang, A. and Bong, C.W.: Antibiotic residues from aquaculture farms and their ecological risks in Southeast Asia: a case study from Malaysia. Ecosyst. Health Sustain., 7: 1926337, 2021. https://doi.org/10.1080/20964129.2021.1926337
  45. Weinstein, M.P. and Lewis, J.S.: The clinical and laboratory standards institute subcommittee on antimicrobial susceptibility testing: Background, organization, functions, and processes. J. Clinc. Microbiol., 58:e01864-19, 2020.
  46. Werner, G., Hildebrandt, B. and Witte, W.: The newly described msrC gene is not equally distributed among all isolates of Enterococcus faecium. Animicrob. Agents Chemother., 45:3672-3673, 2001. https://doi.org/10.1128/AAC.45.12.3672-3673.2001
  47. Woo, S.H., Kim, H.J., Lee, J.S., Kim, J.W. and Park, S.I.: Pathogenicity and classification of streptococci isolated from cultured marine fishes. J. Fish Pathol., 19:17-33, 2006.