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Aeromonas spp. Isolated from Pacific Abalone (Haliotis discus hannai) Marketed in Korea: Antimicrobial and Heavy-Metal Resistance Properties

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Abstract

Antimicrobial and heavy-metal resistance of 29 Aeromonas spp. (Aeromonas hydrophila n = 9, Aeromonas enteropelogenes n = 14, Aeromonas veronii n = 3, Aeromonas salmonicida n = 2, and Aeromonas sobria n = 1) isolated from Pacific abalone marketed in Korea were analyzed. All isolates were found to be resistant against ampicillin. High level of resistant to cephalothin (86%), rifampicin (73%), imipenem (42%), and oxytetracycline (35%) were also detected. Thirteen (45%) of the isolates showed multiple antimicrobial resistance (MAR) index ≥ 0.2. The PCR assays implied the presence of qnrS, qnrB, qnrA, tetB, tetA, aac (3′)- IIa, aac(6′)-Ib, aphAI-IAB, blaCTX, blaTEM, and intI1 genes among 76%, 28%, 14%, 17%, 3%, 3%, 41%, 10%, 41%, 28%, and 66% of the isolates, respectively. Class 1 integron gene cassette profiles aadA1(3%) and aadA2 (3%) were also identified. Lead (Pb) resistance was the highest (69%) among 5 heavy metals tested, whereas 38%, 27%, and 20% of the isolates were resistant to Cadmium (Cd), Chromium (Cr), and Copper (Cu), respectively. Heavy-metal resistance genes, CopA, CzcA, and merA were positive in 83%, 75%, and 41% of the isolates, respectively. In conclusion, observed genotypic and phenotypic resistance profiles of Aeromonas spp. against antimicrobials and heavy metals reveal the ability of serving as a source of antimicrobials and heavy-metal-resistant traits.

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References

  1. Manna SK, Maurye P, Dutta C, Samanta G (2013) Occurrence and virulence characteristics of Aeromonas species in meat, milk and fish in India. J Food Saf 33:461–469

    Google Scholar 

  2. Martins LM, Marquez RF, Yano T (2002) Incidence of toxic Aeromonas isolated from food and human infection. FEMS Immunol Med Mic 32:237–242

    CAS  Google Scholar 

  3. Zhang Q, Shi GQ, Tang GP, Zou ZT, Yao GH, Zeng G (2012) A foodborne outbreak of Aeromonas hydrophila in a college, Xingyi city, Guizhou, China. West Pac Surveill Response J 3:39–45

    CAS  Google Scholar 

  4. Tsheten T, Tshering D, Gyem K, Dorji S, Wangchuk S, Tenzin T, Norbu L, Jamtsho T (2016) An outbreak of Aeromonas hydrophila food poisoning in Deptsang village, Samdrup Jongkhar, Bhutan. J Res Health Sci 16:224–227

    PubMed  PubMed Central  Google Scholar 

  5. De Silva BCJ, Hossain S, Dahanayake PS, Heo GJ (2018) Aeromonas spp. from marketed Yesso scallop (Patinopecten yessoensis): molecular characterization, phylogenetic analysis, virulence properties and antimicrobial susceptibility. J Appl Microbiol 126:288–299

    PubMed  Google Scholar 

  6. Abbott SL, Cheung WKW, Janda JM (2003) The genus Aeromonas: biochemical characteristics, atypical reactions, and phenotypic identification schemes. J Clin Microbiol 41:2348–2357

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Tomás JM (2012) The main Aeromonas pathogenic factors. ISRN Microbiol. https://doi.org/10.5402/2012/256261

    Article  PubMed  PubMed Central  Google Scholar 

  8. Clement M, Olabisi M, David E, Issa M (2019) Veterinary pharmaceuticals and antimicrobial resistance in developing countries. Veterinary Pharmaceuticals IntechOpen. https://doi.org/10.5772/intechopen.84888

  9. UN Environment Programme (2017) Antimicrobial resistance from environmental pollution among biggest emerging health threats, says UN Environment. United Nations Environment Programme. https://www.unenvironment.org/news-and-stories/press-release/antimicrobial-resistance-environmental-pollution-among-biggest. Accessed 15 Jan 2020

  10. Das U (2019) Veterinary public health: the planetary path to one health. In: Yasobant L, Saxena D (eds) Global applications of one health practice and care. IGI Global, Harshey, PA, pp 113–124

    Google Scholar 

  11. Nonejuie P, Burkart M, Pogliano K, Pogliano J (2013) Bacterial cytological profiling rapidly identifies the cellular pathways targeted by antibacterial molecules. PANS 110:16169–16174

    CAS  Google Scholar 

  12. Bharathkumar G, Abraham TJ (2016) Prevalence of transferable oxytetracycline resistance factors in Aeromonas hydrophila in fish hatcheries. FishTechnol 50:324–330

    Google Scholar 

  13. Lupan I, Carpa R, Oltean A, Kelemen BS, Popescu O (2017) Release of antibiotic resistant bacteria by a waste treatment plant from Romania. Microbes Environ 32:219–225

    PubMed  PubMed Central  Google Scholar 

  14. Munita JM, Arias CA, Unit AR, De Santiago A (2016) Mechanisms of antibiotic resistance. Microbiol Spectr 4:1–37

    CAS  Google Scholar 

  15. Lerminiaux NA, Cameron ADS (2018) Horizontal transfer of antibiotic resistance genes in clinical environments. Can J Microbiol 65:34–44

    PubMed  Google Scholar 

  16. Barraud O, Ploy MC (2015) Diversity of class 1 integron gene cassette rearrangements selected under antibiotic pressure. J Bacteriol 197:2171–2178

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Adekanmbi AO, Adelowo OO, Okoh AI, Obasola E (2019) Metal-resistance encoding gene-fingerprints in some bacteria isolated from wastewaters of selected printeries in Ibadan, South-western Nigeria. J Taibah Univ Sci 3655:266–273

    Google Scholar 

  18. Baker-Austin C, Wright MS, Stepanauskas R, Mcarthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14:176–182

    CAS  PubMed  Google Scholar 

  19. Chapman JS (2003) Disinfectant resistance mechanisms, cross-resistance, and co-resistance. Int Biodeterior Biodegrad 51:271–276

    CAS  Google Scholar 

  20. Kamika I, Momba NB (2013) Assessing the resistance and bioremediation ability of selected bacterial and protozoan species to heavy metals in metal-rich industrial wastewater. BMC Microbiol 13:1–14

    Google Scholar 

  21. Seiler C, Berendonk UT (2012) Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Microbiol 3:399–409

    PubMed  PubMed Central  Google Scholar 

  22. Brain RA, Hanson ML, Solomon KR, Brooks BW (2008) Aquatic plants exposed to pharmaceuticals: effects and risks. In: Whitacre DM (ed) Reviews of environmental contamination and toxicology. Springer, New York, pp 67–115

    Google Scholar 

  23. Yonhap News Agency (2017) South Koreans top consumers of seafood: FAO report. https://en.yna.co.kr/view/AEN20170213003800320. Accessed 19 Sept 2019

  24. GLOBEFISH - Information and Analysis on World Fish Trade (2017) Food and Agriculture Organization of the United Nations. https://www.fao.org/in-action/globefish/market-reports/resource-detail/en/c/902597/. Accessed 25 May 2019

  25. Dahanayake PS, 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

    CAS  PubMed  Google Scholar 

  26. Yanez MA, Catalan V, Apraiz D, Figueras MJ (2003) Phylogenetic analysis of members of the genus Aeromonas based on gryB gene sequences. Int J Syst Evol Microbiol 53:875–883

    CAS  PubMed  Google Scholar 

  27. CLSI (2014) Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; twenty‐fourth informational supplement. CLSI Document M100‐S24. CLSI, Wayne, PA

  28. Krumperman PH (1983) Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Appl Environ Microbiol 46:165–170

    CAS  PubMed  PubMed Central  Google Scholar 

  29. He Y, Jin L, Sun F, Hu Q (2016) Antibiotic and heavy-metal resistance of Vibrio parahaemolyticus isolated from fresh shrimps in Shanghai fish markets, China. Environ Sci Pollut Res 23:15033–15040

    CAS  Google Scholar 

  30. Cattoir V, Poirel L, Rotimi V, Soussy CJ (2007) Multiplex PCR for detection of plasmid mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J Antimicrob Chemother 60:394–397

    CAS  PubMed  Google Scholar 

  31. Sunde M, Norstrom M (2005) The genetic background for streptomycin resistance in Escherichia coli influences the distribution of MICs. J Antimicrob Chemother 56:87–90

    CAS  PubMed  Google Scholar 

  32. Samadi N, Pakzad I, Monadi SA, Hosainzadegan H (2015) Study of aminoglycoside resistance genes in Enterococcus and Salmonella strains isolated from Ilam and Milad hospitals. Iran Jundishapur J Microbiol 8:e18102

    PubMed  Google Scholar 

  33. Bouskill NJ, Barnhart EP, Galloway TS, Handy RD (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 60:276–286

    CAS  PubMed  Google Scholar 

  34. Rahman A, Olsson B, Jass J, Nawani N (2007) Genome sequencing revealed chromium and other heavy metal resistance genes in E. cloacae B2-Dha. J Microb Biochem Technol 9:191–199

    Google Scholar 

  35. Vouga M, Greub G (2016) Emerging bacterial pathogens: The past and beyond. Clin Microbiol Infect 22:12–21

    PubMed  Google Scholar 

  36. Shaikh S, Fatima J, Shakil S, Rizvi SMD (2015) Antibiotic resistance and extended spectrum beta-lactamases: types, epidemiology and treatment. Saudi J Biol Sci 22:90–101

    CAS  PubMed  Google Scholar 

  37. Worthington RJ, Melander C (2013) Overcoming resistance to β-lactam antibiotics. J Org Chem 78:4207–4213

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Chen PL, Ko WC, Wu CJ (2012) Complexity of β-lactamases among clinical Aeromonas isolates and its clinical implications. J Microbiol Immunol Infect 45:398–403

    PubMed  Google Scholar 

  39. De Luca F, Giraud-Morin C, Rossolini GM, Docquier JD (2010) Genetic and biochemical characterization of TRU-1, the endogenous class C β-lactamase from Aeromonas enteropelogenes. Antimicrob Agents Chemother 54:1547–1554

    PubMed  PubMed Central  Google Scholar 

  40. Codjoe F, Donkor E (2017) Carbapenem resistance: a review. Med Sci 6:1–28

    Google Scholar 

  41. Li S, Jia X, Li C, Zou H (2018) Carbapenem-resistant and cephalosporin-susceptible Pseudomonas aeruginosa: a notable phenotype in patients with bacteremia. Infect Drug Resist 11:1225–1235

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Hawkey PM, Livermore DM (2012) Carbapenem antibiotics for serious infections. BMJ (Online) 344:1–7

    Google Scholar 

  43. Pfeifer Y, Cullik A, Witte W (2010) Resistance to cephalosporins and carbapenems in Gram-negative bacterial pathogens. Int J Med Microbiol 300:371–379

    CAS  PubMed  Google Scholar 

  44. Adams CA, Austin B, Meaden PG, McIntosh D (1998) Molecular characterization of plasmid-mediated oxytetracycline resistance in Aeromonas salmonicida. Appl Environ Microbiol 64:4194–4201

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Rhodes G, Huys G, Swings J, McGann P (2000) Distribution of oxytetracycline resistance plasmids between aeromonads in hospital and aquaculture environments: implication of Tn1721 in dissemination of the tetracycline resistance determinant tetA. Appl Environ Microbiol 66:3883–3890

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Rôças IN, Siqueira JF (2013) Detection of antibiotic resistance genes in samples from acute and chronic endodontic infections and after treatment. Arch Oral Biol 58:1123–1128

    PubMed  Google Scholar 

  47. Alcaide E, Blasco MD, Esteve C (2010) Mechanisms of quinolone resistance in Aeromonas species isolated from humans, water and eels. Res Microbiol 161:40–45

    CAS  PubMed  Google Scholar 

  48. Wimalasena SHMP, De Silva BCJ, Hossain S, Pathirana HNKS, Heo GJ (2017) Prevalence and characterization of quinolone resistance genes in Aeromonas spp. isolated from pet turtles in South Korea. J Glob Antimicrob Resist 11:34–38

    CAS  PubMed  Google Scholar 

  49. Manchi HM, Kudagi BL, Buchineni M, Jithendra K, Chandra VB, Pathapati RM, Kumar MR, Devi NA (2014) Cephalosporin resistance pattern in a tertiary care hospital—an observation study. Int J Curr Microbiol App Sci 3:718–728

    Google Scholar 

  50. Lee S, Han SW, Kim KW, Song DY, Kwon KT (2014) Third-generation cephalosporin resistance of community-onset Escherichia coli and Klebsiella pneumoniae bacteremia in a secondary hospital. Korean J Intern Med 29:49–56

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Seyedjavadi SS, Sabzehali M, Sabzehali F (2015) Relation between blaTEM, blaSHV and blaCTX-M genes and acute urinary tract infections. J Acute Dis 5:71–76

    Google Scholar 

  52. Yi SW, Chung TH, Joh SJ, Park C (2014) High prevalence of BlaCTX-M group genes in Aeromonas dhakensis isolated from aquaculture fish species in South Korea. J Vet Med Sci 76:1589–1593

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Bali E, Acik L, Sultan N (2014) Phenotypic and molecular characterization of SHV, TEM, CTX-M and extended-spectrum Î2-lactamase produced by Escherichia coli, Acinetobacter baumanii. Afr J Microbiol Res 4:650–654

    Google Scholar 

  54. Gillings MR, Krishnan S, Worden PJ, Hardwick SA (2008) Recovery of diverse genes for class 1 integron-integrases from environmental DNA samples. FEMS Microbiol Lett 287:56–62

    CAS  PubMed  Google Scholar 

  55. Davies J (2007) Microbes have the last word; A drastic re-evaluation of antimicrobial treatment is needed to overcome the threat of antibiotic-resistant bacteria. EMBO Rep 8:616–621

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Bahl MI, Boucher Y, Nesbo CL, Holley M, Stokes HW (2006) Class 1 integrons potentially predating the association with Tn402-Like transposition genes are present in a sediment microbial community. J Bacteriol 188:5722–5730

    PubMed  PubMed Central  Google Scholar 

  57. Agarwal V, Khan MA (2001) Current status of the aadA and dfr gene cassette families. Ann Surg 185:57–65

    Google Scholar 

  58. Mayer KH, Fling ME, Hopkins JD, O’Brien TF (1985) Trimethoprim resistance in multiple genera of Enterobacteriaceae at a U.S. hospital: spread of the type ii dihydrofolate reductase gene by a single plasmid. J Infect Dis 151:783–789

    CAS  PubMed  Google Scholar 

  59. Gillings MR, Gaze WH, Pruden A, Smalla K, Tiedje JM, Zhu YG (2015) Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME J 9:1269–1279

    CAS  PubMed  Google Scholar 

  60. Kang J, Lee YG, Jeong DU, Lee JS, Choi HY (2015) Effect of Abalone farming on sediment geochemistry in the Shallow Sea near Wando, South Korea. Ocean Sci J 50:669–682

    CAS  Google Scholar 

  61. Kang GH, Uhm JY, Choi YG, Kang EK (2018) Environmental exposure of heavy metal (lead and cadmium) and hearing loss: data from the Korea national health and nutrition examination survey (KNHANES 2010–2013). Ann Occup Environ Med 30:1–11

    Google Scholar 

  62. Chen S, Li X, Sun G, Zhang Y (2015) Heavy metal induced antibiotic resistance in bacterium. Int J Mol Sci 16:23390–23404

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Stepanauskas R, Glenn TC, Jagoe CH, Tuckfield RC (2006) Co selection for microbial resistance to metals and antibiotics in freshwater microcosms. Environ Microbiol 8:1510–1514

    CAS  PubMed  Google Scholar 

  64. Berg J, Tom-Petersen A, Nybroe O (2005) Copper amendment of agricultural soil selects for bacterial antibiotic resistance in the field. Lett Appl Microbiol 40:146–151

    CAS  PubMed  Google Scholar 

  65. Llyod NA, Nazaret S, Barkay T (2018) Whole genome sequences to assess the link between antibiotic and metal resistance in three coastal marine bacteria isolated from the mummichog gastrointestinal tract. Mar Pollut Bull 135:514–520

    Google Scholar 

  66. Yang QE, Agouri SR, Tyrrell JM, Walsh TR (2018) Heavy metal resistance genes are associated with blaNDM-1 and blaCTX-M-1-5 carrying Enterobacteriaceae. Antimicrob Agents Chemother 62:e02642–e2717

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Thummeepak R, Pooalai R, Harrison C, Gannon L, Thanwisai A, Chantratita N, Millard AD, Sitthisak S (2020) Essential gene clusters involved in copper tolerance identified in Acinetobacter baumannii clinical and environmental isolates. Pathogens 9:1–16

    Google Scholar 

  68. Naguib MN, El-Gendy AO, Khairalla AS (2018) Microbial diversity of Mer operon genes and their potential rules in mercury bioremediation and resistance. Open Biotechnol J 12:56–77

    CAS  Google Scholar 

  69. Lee IW, Livrelli V, Park SJ, Totis PA, Summers AO (1993) In vivo DNA-protein interactions at the divergent mercury resistance (mer) promoters. II. Repressor/activator (MerR)-RNA polymerase interaction with merOP mutants. J Biol Chem 268:2632–2639

    CAS  PubMed  Google Scholar 

  70. Skurnik D, Ruimy R, Ready D, Ruppe E (2010) Is exposure to mercury a driving force for the carriage of antibiotic resistance genes? J Med Microbiol 59:804–807

    CAS  PubMed  Google Scholar 

  71. Alonso A, Sanchez P, Martinez JL (2001) Environmental selection of antibiotic resistance genes. Environ Microbiol 3:1–9

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Aquatic Animal Medicine, Veterinary Medical Center and College of Veterinary Medicine, Chungbuk National University, Chungdae-ro 1, Seowon-gu, Cheongju, Chungbuk, 28644, Republic of Korea

    M. V. K. S. Wickramanayake, P. S. Dahanayake, Sabrina Hossain & Gang-Joon Heo

  2. College of Veterinary Medicine and Research Institute of Veterinary Medicine, Chungnam National University, Yuseong-gu, Daejeon, 34134, Republic of Korea

    Mahanama De Zoysa

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  1. M. V. K. S. Wickramanayake
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  2. P. S. Dahanayake
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Wickramanayake, M.V.K.S., Dahanayake, P.S., Hossain, S. et al. Aeromonas spp. Isolated from Pacific Abalone (Haliotis discus hannai) Marketed in Korea: Antimicrobial and Heavy-Metal Resistance Properties. Curr Microbiol 77, 1707–1715 (2020). https://doi.org/10.1007/s00284-020-01982-9

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