Dual resistance to heavy metals and antibiotics of Aeromonas hydrophila isolated from Carassius carassius (Linnaeus, 1758) in Lake Tonga, Algeria

Resistance of Aeromonas hydrophila from crucian carp

Authors

DOI:

https://doi.org/10.24193/subbbiol.2023.2.04

Keywords:

Aeromonas hydrophila, Antimicrobial resistance, Carassius carassius, Heavy metal, MAR index

Abstract

Aeromonas hydrophila, a bacterium with significant virulence potential, is the predominant pathogenic bacteria naturally infecting fish. This study aims to identify the antibiogram and heavy metal resistance pattern of Aeromonas hydrophila obtained from both Carassius carassius fish and their surrounding water environment in Lake Tonga, Algeria. A total of 59 strains of Aeromonas hydrophila were isolated from 168 Carassius carassius samples and 144 waters samples of Lake Tonga. All the strains were tested for resistance to 13 antibiotics and three types of heavy metals (Cobalt, copper and cadmium) using disk diffusion and two-fold agar dilution method, respectively.  Clinical macroscopic examination of the fish was also carried out. More than 14% of the examined fishes showed the characteristic clinical signs. Drug screening showed high levels of resistance to β-lactam antibiotics, 100% of the strains were resistant to ampicillin followed by cefalotin (91.53%) and ticarcillin (88.14%). More than 40% of the strains exhibited resistance against gentamicin, amikacin and chloramphenicol. The multiple antibiotic resistance (MAR) indexing of A. hydrophila strains showed that all of them originated from high-risk sources. Among tested heavy metals, bacterial isolates exhibited resistant pattern of Co>Cu >Cd. A positive correlation was observed between antimicrobial resistance and metal tolerance (Odds Ratio>0.1). These resistant profiles could be useful information to avoid unnecessary use of chemical and antimicrobial products in the aquatic environment and to provide a novel approach to manage bacterial infection in fish.

References

Abbott, S.L., Cheung, W.K., & Janda, J.M. (2003). The genus Aeromonas: biochemical characteristics, atypical reactions, and phenotypic identification schemes. J. Clin. Microbiol., 41, 2348–2357. https://dx.doi.org/10.1128/JCM.41.6.2348-2357.2003.

Alcaide, E., Blasco, M.D., & Esteve, C. (2010). Mechanisms of quinolone resistance in Aeromonas species isolated from humans, water and eels. Res. Microbiol., 161, 40-45. http://dx.doi.org/10.1016/j.resmic.2009.10.006

Atef, H.A., El Shafei, H.M., Mansour, M.K., Snosy, S.A.M., & Abo-zaid K.F. (2016). Effect of microbiological contamination and pollution of water on the health status of fish. Eur. J. Acad. Es., 3(5), 178-192.

Asadpour, Y., Barzegar, A., Soleimannezhadbari, E., & Hashempour, A. (2016). Identification of antibiotic and heavy metal susceptibility, bacteria isolated from crayfish (Astacus Leptodactylus) of Aras Dam. Entomol. Appl. Sci. Lett., 3, 2:6-10. Available from: http://nbn-resolving.de/urn:nbn:de:0000easl.v3i2S.944.

Benhalima, L., Amri, S., Bensouilah, M., & Ouzrout, R. (2020). Heavy metal resistance and metallothionein induction in bacteria isolated from Seybouse River, Algeria. Appl. Ecol. Environ. Res., 18, 1721-1737. http://dx.doi.org/10.15666/aeer/1801_17211737

Benhalima, L., Amri, S., Bensouilah, M., & Ouzrout, R. (2019). Antibacterial effect of copper sulfate against multi-drug resistant nosocomial pathogens isolated from clinical samples. Pak. J. Med. Sci., 35(5), 1322-1328. https://doi.org/10.12669/pjms.35.5.336

Cao, Y., Kou, T., Peng, L., Munang’andu, H.M., & Peng, B. (2022). Fructose promotes crucian carp survival against Aeromonas hydrophila Infection. Front. Immunol., 13, 865560. http://dx.doi.org/10.3389/fimmu.2022.865560

Cheng, H., Jiang, H., Fang, J., & Zhu, C. (2019). Antibiotic resistance and characteristics of integrons in Escherichia coli isolated from Penaeus vannamei at a freshwater shrimp farm in Zhejiang Province, China. J. Food Prot., 82, 470-478. http://dx.doi.org/ 10.4315/0362-028X.JFP-18-444

Chettri, U., & Joshi S.R. (2022). A first calibration of culturable bacterial diversity and their dual resistance to heavy metals and antibiotics along altitudinal zonation of the Teesta River. Arch. Microbiol., 204, 241. https://doi.org/10.1007/s00203-022-02858-1

CLSI. (2015). M100-S25 Performance standard for antimicrobial susceptibility testing, twenty-fifth informational supplement, Wayne, PA: Clinical and Laboratory Standards Institute.

Djamai S., Mimeche F., Bensaci E., & Oliva-Paterna F. J. (2019). Diversity of macro-invertebrates in Lake Tonga (northeast Algeria). Biharean Biol., 13 (1), 8-11.

Fang, J., Shen, Y., Qu, D., & Han, J. (2019). Antimicrobial resistance profiles and characteristics of integrons in Escherichia coli strains isolated from a largescale centralized swine slaughterhouse and its downstream markets in Zhejiang, China. Food Control, 95, 215–222. https://doi.org/10.1016/j.foodcont.2018.08.003

Girard, P., & Elie, P. (2007). Manual for the identification of the main anatomo-morphological lesions and external parasites of eels. CEMAGREF/Association “Health Wild Fish”. Cemagref n°110.

González-Fandos, E., & Herrera, B. (2013). Efficacy of propionic acid against Listeria monocytogenes attached to poultry skin during refrigerated storage. Food control, 34, 601-606. https://dx.doi.org/10.1016./j.foodcont.2013.05.034.

Harnisz, M., & Tucholski, S. (2010). Microbial quality of common carp and pikeperch fingerlings cultured in a pondfed with treated wastewater. Ecol. Eng., 36, 466-470. https://dx.doi.org/10.1016/j.ecoleng.2009.11.015.

Jiang, M., Yang L-F., Zheng, J., Chen Z.G., & Peng B. (2020). Maltose promotes crucian carp survival against Aeromonas sobrial infection at high temperature. Virulence, 11(1), 877-888. https://dx.doi.org/10.1080/21505594.2020.1787604

Jiang, H., Yu, T., Yang, Y., Yu, S., Wu, J., Lin, R., Li, Y., Fang, J., & Zhu, C. (2020). Co-occurrence of antibiotic and heavy metal resistance and sequence type diversity of Vibrio parahaemolyticus isolated From Penaeus vannamei at freshwater farms, seawater farms, and markets in Zhejiang Province, China. Front. Microbiol., 11, 1294. https://dx.doi.org/10.3389/fmicb.2020.01294

Lee, S.W. & Wendy, W. (2017). Antibiotic and heavy metal resistance of Aeromonas hydrophila and Edwardsiella tarda isolated from red hybrid tilapia (Oreochromis spp.) coinfected with motile aeromonas septicemia and edwardsiellosis. Vet. World, 10(7), 803-807. https://dx.doi.org/10.14202/vetworld.2017.803-807

Liu, Y.S., Deng, Y., Chen, C.K., Khoo, B.L. , & Chua, S.L. (2020). Rapid detection of microorganisms in a fish infection microfluidics platform. J. Hazard. Mater., 431, 128572. https://doi.org/10.1016/j.jhazmat.2022.128572

Lü, A.J., Hu, X.C., Li, L., Sun, J.F., Song, Y.J., Pei, C., Zhang, C., & Kong, X.H. (2016). Isolation, identification and antimicrobial susceptibility of pathogenic Aeromonas media isolated from diseased Koi carp (Cyprinus carpio koi). Iran. J. Fish. Sci., 15, 760-774. Available from: https://jifro.ir/article-1-2219-en.html

Michel, C., Kerouault, B., & Martin, C. (2003). Chloramphenicol and florfenicol suceptibility of fish-pathogenic bacteria isolated in France: comparison of minimum inhibitory concentration, using recommended provisory standards for fish bacteria. J. Appl. Microbiol., 95, 1008–1015. http://dx.doi.org/10.1046/j.1365-2672.2003.02093.x.

Olumide, A.O., & Asmat, A. (2015). Antibiotic resistance profiling and phenotyping of Aeromonas species isolated from aquatic sources. Saudi J. Biol. Sci., 65-70. http://dx.doi.org/10.1016/j.sjbs.2015.09.016

Outa, J.O., Kowenje, C.O., & Avenant-Oldewage, A. (2020). Trace Elements in Crustaceans, Mollusks and Fish in the Kenyan Part of Lake Victoria: Bioaccumulation, Bioindication and Health Risk Analysis. Arch. Environ. Contam. Toxicol., 78, 589-603 https://doi.org/10.1007/s00244-020-00715-0

Sarter, S., Kha Nguyen, H.N., Hung, L.T., Lazard, J., & Montet, D. (2007). Antibiotic resistance in Gram-negative bacteria isolated from farmed catfish. Food Control, 18, 1391-1396. http://dx.doi.org/10.1016/j.foodcont.2006.10.003

Shamsun, N., Mizanur Rahman, M., Uddin Ahmed, G., & Reza Faruk M.A. (2016). Isolation, identification, and characterization of Aeromonas hydrophila from juvenile farmed pangasius (Pangasianodon hypophthalmus). Int. J. Fish. Aqua. Stud., 4, 52-60. Available from: http://www.fisheriesjournal.com/archives/2016/vol4issue4/PartA/4-3-32-237.pdf.

Shao-wu, L., Wang, D., Hong-bai, L., & Tong-yan, L. (2013). Molecular Typing of Aeromonas hydrophila Isolated from Common Carp in Northeast China. J. Northeast Agric. Univ., 20, 30-36. https://doi.org/10.1016/S1006-8104(13)60005-7

Shuvho, C.B., Fabaya, R., Ali Reza, A.K.M., Sharifa Khatun, M., Luthful Kabir, M., Hafizur Rahman, M., & Shirajum Monir, M. (2016). Isolation, molecular identification and antibiotic susceptibility profile of Aeromonas hydrophila from cultured indigenous Koi (Anabus testudineus) of Bangladesh. Asian J. Med. Biol. Res., 2(2), 332-340. http://dx.doi.org/10.3329/ajmbr.v2i2.29078

Stratev, D., & Odeyemib, O.A. (2016). Antimicrobial resistance of Aeromonas hydrophila isolated from different food sources: A mini-review. J. Infec. Public Health, 9, 535-544. http://dx.doi.org/10.1016/j.jiph.2015.10.006

Resende, J. A., Silva, V.L., Fontes, C.O., Souza-Filho, J.A., Rocha De Oliveira, T.L., Coelho, C.M., César ,D.E., & Diniz, C.G. (2012). Multidrug-resistance and toxic metal tolerance of medically important bacteria isolated from an aquaculture system. Microbes Environ., 27(4), 449–455. http://dx.doi.org/10.1264/jsme2.ME12049

Pathak, S.P., & Gopal, K. (2009). Bacterial density and antibiotic resistance of Aeromonas sp. in organs of metal-stressed freshwater fish Channa punctatus, Toxicol. Environ. Chem., 91(2), 331-337. http://dx.doi.org/10.1080/02772240802098222

Pfeifer, Y., Cullik, A., & Witte, W. (2010). Resistance to cephalosporins and carbapenems in Gram-negative bacterial pathogens. Inter. J. Med. Microbiol., 300, 371–379. http://dx.doi.org/10.1016/j.ijmm.2010.04.005

Shuvho, C.B., Fabaya, R., Ali Reza, A.K.M., Sharifa Khatun, M., Luthful Kabir, M., Hafizur Rahman, M., & Shirajum Monir, M. (2016). Isolation, molecular identification and antibiotic susceptibility profile of Aeromonas hydrophila from cultured indigenous Koi (Anabus testudineus) of Bangladesh. Asian J. Med. Biol. Res., 2(2), 332-340. http://dx.doi.org/10.3329/ajmbr.v2i2.29078.

Sollid, J., De Angelis, P., Gundersen, K., & Nilsson, E. G. (2003). Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. J. Exp. Biol., 206, 3667-3673. http://dx.doi.org/10.1242/jeb.00594

Vivekanandhan, G., Savithamani, K., Hatha, A.A.M, & Lakshmanaperumalsamy, P. (2002). Antibiotic resistance of Aeromonas hydrophila isolated from marketed fish and prawn of South India. Int. J. Food Microbiol., 76, 165–168. PMID: 12038573

Wei, L.S., Mustakim, M.T., Azlina, I.N., Zulhisyam, A.K., Anamt, M.N., Wee, W., & Huang, N.M. (2015). Antibiotic and heavy metal resistance of Aeromonas spp. isolated from diseased red hybrid tilapia (Oreochromis sp.). Ann. Res. Rev. Biol., 6, 264–269.

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

Yi, S.W., Kim, D.C., You, M.J., Kim, B.S., Kim, W.I., Yi, S.W., & Shin, G.W. (2014). Antibiotic and heavy-metal resistance in motile Aeromonas strains isolated from fish. Afr. J. Microbiol. Res., 8, 1793–1797. https://dx.doi.org/10.5879/AJMR2013.6339

Yu, Z., Gunn, L., Wall, P., & Fanning, S. (2017). Antimicrobial resistance and its association with tolerance to heavy metals in agriculture production. Food Microbiol., 64, 23-32. https://dx.doi.org/10.1016/j.fm.2016.12.009

Zdanowicz, M., Mudryk, Z.J., & Perliński, P. (2020). Abundance and antibiotic resistance of Aeromonas isolated from the water of three carp ponds. Vet. Res. Commun., 44, 9–18. https://doi.org/10.1007/s11259-020-09768-x

Zhang, D., Xu, D.H., & Shoemaker, C. (2016). Experimental induction of motile Aeromonas septicemia in channel cat¬fish (Ictalurus punctatus) by waterborne challenge with vir¬ulent Aeromonas hydrophila. Aquac. Rep., 3, 18-23. https://doi.org/10.1016/j.aqrep.2015.11.003

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2023-12-27

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