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Detection of virulence, antimicrobial resistance, and heavy metal resistance properties in Vibrio anguillarum isolated from mullet (Mugil cephalus) cultured in Korea

  • Veterinary Microbiology - Research Paper
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Abstract

In the present study, we identified and characterized 22 strains of V. anguillarum from 145 samples of mullets (Mugill cephallus) cultured in several fish farms in South Korea. They were subjected to pathogenicity tests, antimicrobial susceptibility test, and broth dilution test to detect virulence markers, antimicrobial resistance, and heavy metal resistance properties. All the isolates showed amylase and caseinase activity, followed by gelatinase (90.9%), DNase (45.5%), and hemolysis activities (α = 81.1% and β = 18.2%). The PCR assay revealed that isolates were positive for VAC, ctxAB, AtoxR, tdh, tlh, trh, Vfh, hupO, VPI, and FtoxR virulence genes at different percentages. All the isolates showed multi-drug resistance properties (MAR index ≥ 0.2), while 100% of the isolates were resistant to oxacillin, ticarcillin, streptomycin, and ciprofloxacin. Antimicrobial resistance genes, qnrS (95.5%), qnrB (86.4%), and StrAB (27.3%), were reported. In addition, 40.9% of the isolates were cadmium-tolerant, with the presence of CzcA (86.4%) heavy metal resistance gene. The results revealed potential pathogenicity associated with V. anguillarum in aquaculture and potential health risk associated with consumer health.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References 

  1. Organisation for Economic Co-operation and Development (2021) Fisheries and aquaculture in Korea. OECD review of fisheries country notes, Korea. Retrieved from https://www.oecd.org/agriculture/topics/fisheries-and-aquaculture/documents/report_cn_fish_kor.pdf. Accessed 12 Oct 2022

  2. Ko EY, Park JO, Lee KS (2019) Review of fish name on the fishes of the family Mugilidae in Korea and resource utilization. J Mar Life Sci 4(2):96–105. https://doi.org/10.23005/KSMLS.2019.4.2.96

    Article  Google Scholar 

  3. World Wide Fund for Nature (2016) Korea’s fisheries sector assessment. WWF-Korea. Retrieved from http://www.wwfkorea.or.kr/data/file/english_report/3554271915_gOcBYZPk_5086a59a1852f5d1166c8f523efdfbc9007f532b.pdf. Accessed 10 Oct 2022

  4. Food and Agriculture Organization of the United Nations (2022) The state of world fisheries and aquaculture. FAO. Retrieved from https://www.fao.org/3/cc0461en/cc0461en.pdf. Accessed 12 Oct 2022

  5. Naka H, Crosa JH (2011) Genetic determinants of virulence in the marine fish pathogen Vibrio anguillarum. Fish Pathol 46:1–10. https://doi.org/10.3147/jsfp.46.1

    Article  PubMed  PubMed Central  Google Scholar 

  6. Akinbowale OL, Peng H, Grant P, Barton MD (2007) Antibiotic and heavy metal resistance in motile aeromonads and pseudomonads from rainbow trout (Oncorhynchus mykiss) farms in Australia. Int J Antimicrob Agents 30:177–182. https://doi.org/10.1016/j.ijantimicag.2007.03.012

  7. Ransangan J, Mustafa S (2009) Identification of Vibrio harveyi isolated from diseased Asian Seabass Lates calcarifer by use of 16S ribosomal DNA sequencing. J aquat Anim Health 21(3):150–155. https://doi.org/10.1577/H09-002.1

    Article  PubMed  Google Scholar 

  8. Aoki T, Satoh T, Kitao T (1987) New tetracycline resistance determinant on R plasmids from Vibrio anguillarum. Antimicrob Agents Chemother 31(9):1446–1449. https://doi.org/10.1128/aac.31.9.1446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Sinatra JA, Colby K (2018) Notes from the field: fatal Vibrio anguillarum infection in an immunocompromised patient- Maine 2017. MMWR Morb Mortal Wkly Rep 67(34):962–963

    Article  Google Scholar 

  10. Kim SW, Kim JO, Kim WS (2014) Vibrio anguillarum infection in rainbow trout (Oncorhynchus mykiss) during seawater adaption. J fish Pathol 27(2):133–137. https://doi.org/10.7847/jfp.2014.27.2.133

    Article  Google Scholar 

  11. Toranzo AE, Barja JL (1990) A review of the taxonomy and seroepizootiology of Vibrio anguillarum, with special reference to aquaculture in the northwest of Spain. Dis aquat Org 9:73–82

    Article  Google Scholar 

  12. Burke J, Rodgers L (1981) Identification of pathogenic bacteria associated with the occurrence of ‘red spot’ in sea mullet, Mugil cephalus L., in south-eastern Queensland. J Fish Dis 4(2):153–159. https://doi.org/10.1111/j.1365-2761.1981.tb01119.x

    Article  Google Scholar 

  13. Amany AA, Mona MS (2005) Vibriosis in some fishes molecular characterization of fish pathogenic vibrios. Vet Med J 53(4):911–923

    Google Scholar 

  14. Huang L, Gao Q, Zhang Y (2021) Community change and pathogenicity of Vibrio. In: Neri V, Huang L, Li J (eds) Infections and sepsis development. IntechOpen, London, pp 268–290

    Google Scholar 

  15. Frans I, Michiels CW, Bossier P, Willems K, Lievens B, Rediers H (2011) Vibrio anguillarum as a fish pathogen: virulence factors, diagnosis and prevention. J fish dis 34(9):643–661. https://doi.org/10.1111/j.1365-2761.2011.01279.x

    Article  CAS  PubMed  Google Scholar 

  16. Pedersen BK, Tiainen T, Larsen JL (1995) Antibiotic resistance of Vibrio anguillarum, in relation to serovar and plasmid contents. Acta Vet Scand 36:55–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Parin U, Erbas G, Yuksel Savasan S, HT, Gurpinar S and Kirkan S, (2017) Antimicrobial resistance of Vibrio (Listonella) anguillarum isolated from rainbow trouts (Oncorhynchus mykiss). Indian J Anim Res 53(11):1522–1525. https://doi.org/10.18805/ijar.v0iOF.7251

    Article  Google Scholar 

  18. Eom SY, Lee YS, Lee SG, Seo MN, Choi BS, Kim YD, Lim J, Hwang MS (2017) Lead, mercury, and cadmium exposure in the Korean general population. J Korean Med Sci 33:e9. https://doi.org/10.3346/jkms.2018.33.e9

    Article  CAS  PubMed Central  Google Scholar 

  19. Dahanayake P, Hossain S, Wickramanayake MVKS, Heo GJ (2019) Antibiotic and heavy metal resistance genes in Aeromonas spp. isolated from marketed Manila clam (Ruditapes philippinarum) in Korea. J Appl Microbiol 127:941–952. https://doi.org/10.1111/jam.14355

    Article  CAS  PubMed  Google Scholar 

  20. Matyar F, Kaya A (2008) Antibacterial agents and heavy metal resistance in Gram-negative bacteria isolated from seawater, shrimp and sediment in Iskenderun Bay. Turkey Sci Total Environ 407(1):279–285. https://doi.org/10.1016/j.scitotenv.2008.08.014

    Article  CAS  PubMed  Google Scholar 

  21. Farmer JJ, Janda JM (2005) Family Vibrionaceae. In: Brenner BJ, Krieg NR, Staley JT (eds) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, New York, pp 491–494

    Google Scholar 

  22. Kim H, Ryu J, Lee S, Kim E, Kim H (2015) Multiplex PCR for detection of the Vibrio genus and five pathogenic Vibrio species with primer sets designed using comparative genomics. BMC Microbiol 15(2015):239. https://doi.org/10.1186/s12866-015-0577-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Hong G, Kim D, Bae J, Ahn S, Bai SC, Kong I (2007) Species-specific PCR detection of the fish pathogen, Vibrio anguillarum, using the amiB gene, which encodes N-acetylmuramoyl-L-alanine amidase. FEMS Microbiol Lett 269(2):201–206. https://doi.org/10.1111/j.1574-6968.2006.00618.x

    Article  CAS  PubMed  Google Scholar 

  24. Zhang X, Austin B (2000) Pathogenicity of Vibrio harveyi to salmonids. J Fish Dis 23(2):93–102. https://doi.org/10.1046/j.1365-2761.2000.00214.x

  25. Liu P, Lee K, Chen S (1996) Pathogenicity of different isolates of Vibrio harveyi in tiger prawn. Penaeus monodon Lett Appl Microbiol 22(6):413–416. https://doi.org/10.1111/j.1472-765X.1996.tb01192.x

    Article  Google Scholar 

  26. Rodrigues DP, Ribeiro RV, Alves RM et al (1993) Evaluation of virulence factors in environmental isolates of Vibrio species. Mem I Oswaldo Cruz 88(4):589–592. https://doi.org/10.1590/s0074-02761993000400016

    Article  CAS  Google Scholar 

  27. Freeman DJ, Falkiner FR, Patrick S (1989) New method for detecting slime production by coagulase negative staphylococci. J Clin Pathol 42(8):872–874. https://doi.org/10.1136/jcp.42.8.872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. CLSI (2020) Clinical and Laboratory Standards Institute, Performance standards for antimicrobial susceptibility testing; twenty-fourth information supplement M100-S24, CLSI, Wayne, Pa, USA

  29. Adenaike O, Olonitola OS, Ameh WCMZ (2016) Multidrug resistance and multiple antibiotic resistance index of Escherichia coli strains isolated from retailed smoked fish. J Nat Sci Res 6(9):7–10

    Google Scholar 

  30. He Y, Jin L, Sun F et al (2016) Antibiotic and heavy-metal resistance of Vibrio parahaemolyticus isolated from fresh shrimps in Shanghai fish markets. China Res Int 23(15):15033–15040. https://doi.org/10.1007/s11356-016-6614-4

    Article  CAS  Google Scholar 

  31. Bej AK, Patterson DP, Brasher CW, Vickery MCL, Jones DD, Kaysner CA (1999) Detection of total and hemolysin-producing Vibrio parahaemolyticus in shellfish using multiplex PCR amplification of tl, tdh and trh. J Microbiol 36:215–225. https://doi.org/10.1016/s0167-7012(99)00037-8

    Article  CAS  Google Scholar 

  32. Liang P, Cui X, Du X et al (2013) The virulence phenotypes and molecular epidemiological characteristics of Vibrio fluvialis in China. Gut Pathogens 5(1):6. https://doi.org/10.1186/1757-4749-5-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Chakraborty R, Sinha S, Mukhopadhyay AK et al (2006) Species-specific identification of Vibrio fluvialis by PCR targeted to the conserved transcriptional activation and variable membrane tether regions of the toxR gene. J M Microbiol 55(6):805–808. https://doi.org/10.1099/jmm.0.46395-0

    Article  Google Scholar 

  34. Xie ZY, Hu CQ, Chen C et al (2005) Investigation of seven Vibrio virulence genes among Vibrio alginolyticus and Vibrio parahaemolyticus strains from the coastal mariculture systems in Guangdong. China Lett Appl Microbiol 41(2):202–207. https://doi.org/10.1111/j.1472-765X.2005.01688.x

    Article  CAS  PubMed  Google Scholar 

  35. Hossain S, Wickramanayake MVKS, Dahanayake PS et al (2020) Occurrence of virulence and extended-spectrum β-lactamase determinants in Vibrio spp. isolated from marketed hard-shelled mussel (Mytilus coruscus). Microb Drug Resist 26(4):391–401. https://doi.org/10.1089/mdr.2019.0131

    Article  CAS  PubMed  Google Scholar 

  36. De Silva LADS, Wickramanayake MVKS, Heo GJ (2022) Occurrence of virulence and antimicrobial resistance determinants in Vibrio harveyi isolated from marine food fish cultured in Korea. Microb Drug Resist 28(2):255–265. https://doi.org/10.1089/mdr.2020.0618

    Article  CAS  PubMed  Google Scholar 

  37. Wimalasena SHMP, De Silva BCJ et al (2017) Prevalence and characterization of quinolone resistance genes in Aeromonas species isolated from pet turtle in Korea. J Glob Antimicrob Resist 11:34–38. https://doi.org/10.1016/j.jgar.2017.06.001

    Article  CAS  PubMed  Google Scholar 

  38. Bouskill NJ, Barnhart EP, Galloway TS et al (2007) Quantification of changing Pseudomonas aeruginosa sodA, htpX and mt gene abundance in response to trace metal toxicity: a potential in situ biomarker of environmental health. FEMS Microbiol Ecol 60(2):276–286. https://doi.org/10.1111/j.1574-6941.2007.00296.x

    Article  CAS  PubMed  Google Scholar 

  39. De Silva BCJ, Hossain S, Dahanayake PS et al (2018) Frozen white-leg shrimp (Litopenaeus vannamei) in Korean markets as a source of Aeromonas spp harboring antibiotic and heavy metal resistance genes. Microb Drug Resist 24(10):1587–1598. https://doi.org/10.1089/mdr.2018.0035

    Article  CAS  PubMed  Google Scholar 

  40. Park K, Mok JS, Kwon JY et al (2018) Food-borne outbreaks, distributions, virulence, and antibiotic resistance profiles of Vibrio parahaemolyticus in Korea from 2003 to 2016: a review. Fish Aquatic Sci 21:3. https://doi.org/10.1186/s41240-018-0081-4

    Article  CAS  Google Scholar 

  41. Santos Y, Bandín I, Nún˜ez S, et al (1992) Comparison of the extracellular biological activities of Vibrio anguillarum and Aeromonas hydrophila. Aquaculture 2(3):259–270. https://doi.org/10.1016/0044-8486(92)90075-v

    Article  Google Scholar 

  42. Ma L, Chen J, Liu R et al (2009) Mutation of rpoS gene decreased resistance to environmental stresses, synthesis of extracellular products and virulence of Vibrio anguillarum. FEMS Microbiol Ecol 70(2):286–292. https://doi.org/10.1111/j.1574-6941.2009.00713.x

    Article  CAS  Google Scholar 

  43. Younes AM, Gaafar A (2021) Prevalence of pathogenic Vibrio anguillarum among Oreochromisniloticus fish fingerlings infected with saprolegniasis around Qarun Lake. Egypt J Vet Sci 52(2):257–266. https://doi.org/10.21608/ejvs.2021.67242.1222

    Article  Google Scholar 

  44. Costa RA, Amorim LMC, Araujo RL et al (2013) Multiple enzymatic profiles of Vibrio parahaemolyticus strains isolated from oysters. Rev Argent Microbiol 45(4):267–270. https://doi.org/10.1016/S0325-7541(13)70035-X

    Article  CAS  PubMed  Google Scholar 

  45. Miyoshi S (2013) Extracellular proteolytic enzymes produced by human pathogenic Vibrio species. Front Microbiol 4:1–8. https://doi.org/10.3389/fmicb.2013.00339

    Article  Google Scholar 

  46. Vergis EN, Shankar N, Chow JW et al (2002) Association between the presence of Enterococcal virulence factors gelatinase, hemolysin, and enterococcal surface protein, and mortality among patients with bacteremia due to Enterococcus faecalis. Clin Infect Dis 35(5):570–575. https://doi.org/10.1086/341977

    Article  CAS  PubMed  Google Scholar 

  47. Park MY, Kim HJ, Choi ST et al (2003) Pathogenic factors of Vibrio spp. isolated from seawater of Gwangan beach in Busan. J Fish Sci Tech 5(3):178–182

    Google Scholar 

  48. Hernandez-Robles MF, Natividad-Bonifacio I, Alvarez-Contreras AK, Tercero-Alburo JJ, Quiones-Ramırez EI, Vazquez-Salinas C (2021) Characterization of potential virulence factors of Vibrio mimicus isolated from fishery products and water. Int J Microbiol 2021. https://doi.org/10.1155/2021/8397930

  49. Schroeder M, Brooks BD, Brooks AE (2017) The complex relationship between virulence and antibiotic resistance. Genes 8(1):39. https://doi.org/10.3390/genes8010039

    Article  CAS  PubMed Central  Google Scholar 

  50. Hossain S, Vidanalage M, Sameera K et al (2020) Occurrence of virulence and extended-spectrum β-lactamase determinants in Vibrio spp isolated from marketed hard-shelled mussel (Mytilus coruscus). 26(4):391–401. https://doi.org/10.1089/mdr.2019.0131

    Article  CAS  Google Scholar 

  51. Sabrina H, De Siva BCJ, Dahanayake PS et al (2019) Vibrio spp. from Yesso scallop (Patinopecten yessoensis) demonstrating virulence properties and antimicrobial resistance. J Food Saf 39(3):e12634. https://doi.org/10.1111/jfs.12634

    Article  CAS  Google Scholar 

  52. Deng Y, Xu L, Chen H, Liu S, Guo Z, Cheng C, Ma H, Feng J (2020) Prevalence, virulence genes, and antimicrobial resistance of Vibrio species isolated from diseased marine fish in South China. Sci Rep 10(1):1–8. https://doi.org/10.1038/s41598-020-71288-0

    Article  CAS  Google Scholar 

  53. Waldor MK, Mekalanos JJ (1996) Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272(5270):1910–1914. https://doi.org/10.1126/science.272.5270.1910

    Article  CAS  PubMed  Google Scholar 

  54. Okuda J, Nakai T, Chang PS et al (2001) The toxR gene of Vibrio (Listonella) anguillarum controls expression of the major outer membrane proteins but not virulence in a natural host model. Infect Immun 69(10):6091–6101. https://doi.org/10.1128/IAI.69.10.6091-6101.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Singhapol C, Tinrat S (2020) Virulence genes analysis of Vibrio parahaemolyticus and anti-vibrio activity of the citrus extracts. Curr Microbiol 77:1390–1398

    Article  CAS  PubMed  Google Scholar 

  56. Khalil SA, Abou-akkada AS, El-hoshy SM (2014) Molecular studies on Vibrio species isolated from imported frozen fish. Global Veterinaria 12(6):782–789. https://doi.org/10.5829/idosi.gv.2014.12.06.83316

    Article  CAS  Google Scholar 

  57. Sadat A, El-Sherbiny H, Zakaria A et al (2021) Prevalence, antibiogram and virulence characterization of Vibrio isolates from fish and shellfish in Egypt: a possible zoonotic hazard to humans. J Appl Microbiol 131(1):485–498. https://doi.org/10.1111/jam.14929

    Article  CAS  PubMed  Google Scholar 

  58. Doris YW, Di AL, Jeonghwan J et al (2016) Season-specific occurrence of potentially pathogenic Vibrio spp. on the southern coast of South Korea. Appl Environ Microbiol 83(3):e02680. https://doi.org/10.1128/AEM.02680-16

    Article  Google Scholar 

  59. Fri J, Ndip RN, Njom HA et al (2017) Occurrence of virulence genes associated with human pathogenic vibrios isolated from two commercial dusky kob (Argyrosmus japonicus) farms and Kareiga estuary in the Eastern Cape Province, South Africa. Int J Environ Res Public Health 14(10):1111. https://doi.org/10.3390/ijerph14101111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Gxalo O, Digban TO, Igere BE et al (2021) Virulence and antibiotic resistance characteristics of Vibrio isolates from rustic environmental freshwaters. Front Microbiol 11:1–12. https://doi.org/10.3389/fcimb.2021.732001

    Article  CAS  Google Scholar 

  61. World Health Organization (2021) Antimicrobial resistance. WHO. https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance. Accessed 22 Oct 2022

  62. Tendencia EA, Dela Peña LD (2002) Level and percentage recovery of resistance to oxytetracycline and oxolinic acid of bacteria from shrimp ponds. Aquaculture 213:1–13. https://doi.org/10.1016/S0044-8486(02)00017-0

    Article  CAS  Google Scholar 

  63. Zago V, Veschetti L, Patuzzo C et al (2020) Resistome, mobilome and virulome analysis of Shewanella algae and Vibrio spp. strains isolated in Italian aquaculture centers. Microorganisms 8(4):572. https://doi.org/10.3390/microorganisms8040572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Vaseeharan B, Ramasamy P, Murugan T (2005) In vitro susceptibility of antibiotics against Vibrio spp. and Aeromonas spp. isolated from Penaeus monodon hatcheries and ponds. Int J Antimicrob Agents 26(4):285–291. https://doi.org/10.1016/j.ijantimicag.2005.07.005

    Article  CAS  PubMed  Google Scholar 

  65. Papp-Wallace KM, Endimiani A, Taracila MA et al (2011) Carbapenems: past, present, and future. Antimicrob Agents Chemother 55(11):4943–4960. https://doi.org/10.1128/AAC.00296-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Miranda CD, Kehrenberg C, Ulep C et al (2003) Diversity of tetracycline resistance genes in bacteria from Chilean salmon farms. Antimicrob Agents Chemother 47(3):883–888. https://doi.org/10.1128/AAC.47.3.883-888.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. McMillan EA, Gupta SK, Williams LE et al (2019) Antimicrobial resistance genes, cassettes, and plasmids present in Salmonella enterica associated with United States food animals. Front Microbiol 10:832. https://doi.org/10.3389/fmicb.2019.00832

    Article  PubMed  PubMed Central  Google Scholar 

  68. Zhang Z, Zhang Q, Wang T et al (2022) Assessment of global health risk of antibiotic resistance genes. Nat Commun 13:1553. https://doi.org/10.1038/s41467-022-29283-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Jacoby GA, Strahilevitz J, Hooper DC (2015) Plasmid-mediated quinolone resistance. Microbiol Spectr 2(2):475–503. https://doi.org/10.1128/microbiolspec

    Article  Google Scholar 

  70. Strahilevitz J, Jacoby GA, Hooper DC et al (2009) Plasmid-mediated quinolone resistance: a multifaceted threat. Clin Microbiol Rev 22(4):664–689. https://doi.org/10.1128/CMR.00016-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Martínez JL (2019) Mechanisms of action and of resistance to quinolones. Antibiot Drug Resist 2(1):40–61. https://doi.org/10.1111/j.1751-7915.2008.00063.x

    Article  CAS  Google Scholar 

  72. Rojas MVR, Matté MH, Dropa M et al (2011) Characterization of Vibrio Parahaemolyticus isolated from oysters and mussels in São Paulo Brazil. Rev Inst Med Trop Sao Paulo 53(4):201–205. https://doi.org/10.1590/s0036-46652011000400005

    Article  PubMed  Google Scholar 

  73. Ye L, Li R, Lin D et al (2016) Characterization of an IncA/C multidrug resistance plasmid in Vibrio alginolyticus. Antimicrob Agents Chemother 60(5):3232–3235. https://doi.org/10.1128/AAC.00300-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Hall RM, Stokes HW (1993) Integrons: novel DNA elements which capture genes by site-specific recombination. Genetica 90(2–3):115–132. https://doi.org/10.1007/BF01435034

    Article  CAS  PubMed  Google Scholar 

  75. Jeamsripong S, Khant W, Chuanchuen R (2020) Distribution of phenotypic and genotypic antimicrobial resistance and virulence genes in Vibrio parahaemolyticus isolated from cultivated oysters and estuarine water. FEMS Microbiol Ecol 96(8):fiaa08. https://doi.org/10.1093/femsec/fiaa081

    Article  CAS  Google Scholar 

  76. Barlow RS, Pemberton JM, Desmarchelier PM et al (2004) Isolation and characterization of integron-containing bacteria without antibiotic selection. Antimicrob Agents Chemother 48(3):838–842. https://doi.org/10.1128/AAC.48.3.838-842.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Adekanmbi AO, Adelowo OO, Okoh AI et al (2019) Metal resistance encoding gene-fingerprints in some bacteria isolated from wastewaters of selected printeries in Ibadan. South-western Nigeria J Taibah Univ Sci 13(1):266–273. https://doi.org/10.1080/16583655.2018.1561968

    Article  Google Scholar 

  78. Baker-Austin C, Wright MS, Stepanauskas R et al (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14(4):176–182. https://doi.org/10.1016/j.tim.2006.02.006

    Article  CAS  PubMed  Google Scholar 

  79. Su J, Zhang Y, Hu T, Ming H, Xie Y, Jin Y, Shi T, Fan J (2022) Prevalence, antibiotic and heavy metal resistance of Vibrio spp. isolated from the clam Meretrix meretrix at different ages in Geligang, Liaohe estuary in China. Front Mar Sci 2022(9): 1–10. https://doi.org/10.3389/fmars.2022.1071371

  80. Kang CH, Shin YJ, Yu HS et al (2018) Antibiotic and heavy-metal resistance of Vibrio parahaemolyticus isolated from oysters in Korea. Mar Pollut Bull 135:69–74. https://doi.org/10.1016/j.marpolbul.2018.07.007

    Article  CAS  PubMed  Google Scholar 

  81. Svanevik CS, Urdahl AM, Lunestad BT, Norström M, Slettemeås JS, Nilsen H, Storesund J (2021) Screening for antimicrobial- and heavy metal resistant bacteria in copper contaminated areas. Institute of Marine Research M1925:1-42. https://www.hi.no/en/hi/nettrapporter/rapport-fra-havforskningen-en-2021-18. Accessed 12 Oct 2022

  82. Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339. https://doi.org/10.1016/S0168-6445(03)00048-2

    Article  CAS  PubMed  Google Scholar 

  83. Deredjian A, Colinon C, Brothier E et al (2011) Antibiotic and metal resistance among hospital and outdoor strains of Pseudomonas aeruginosa. Res Microbiol 162(7):689–700. https://doi.org/10.1016/j.resmic.2011.06.007

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We appreciate Professor Shin Gee-Wook of Chonbuk National University’s Bio-Safety Research Institute and College of Veterinary Medicine in South Korea for providing the bacterial strains utilized in this investigation.

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PMK and GJH contributed to the conception and design of the study. Material preparation, data collection, and analysis were performed by PMK, SM, LADSDS, and GJH. The first draft of the manuscript was written by PMK, and all authors contributed to reviewing and editing the manuscript. All authors read and approved the final manuscript.

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Correspondence to Gang-Joon Heo.

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Kumarage, P.M., Majeed, S., De Silva, L.A.D.S. et al. Detection of virulence, antimicrobial resistance, and heavy metal resistance properties in Vibrio anguillarum isolated from mullet (Mugil cephalus) cultured in Korea. Braz J Microbiol 54, 415–425 (2023). https://doi.org/10.1007/s42770-023-00911-9

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