Abstract
The aim of the present study was to determine the level of antibiotic resistance patterns and distribution of heavy metal resistance of bacterial isolates from aquatic animals (Lissotriton vulgaris, Pelophylax ridibundus, Emys orbicularis, Mauremys rivulata, and Natrix natrix) in Turkey (Kavak Delta). A total of 153 bacteria have been successfully isolated from cloaca and oral samples of the aquatic amphibians and reptilians which were found, namely, Aeromonas sp. (n = 29), Plesiomonas sp. (n = 7), Vibrio sp. (n = 12), Citrobacter sp. (n = 12), Enterobacter sp. (n = 11), Escherichia sp. (n = 22), Klebsiella sp. (n = 22), Edwardsiella sp. (n = 6), Hafnia sp. (n = 1), Proteus sp. (n = 19), Providencia sp. (n = 8), and Pseudomonas sp. (n = 4). In terms of antibiotic and heavy metal susceptibility testing, each isolate was tested against 12 antibiotics and 4 metals. There was a high incidence of resistance to cefoxitin (46.40 %), ampicillin (44.44 %), erythromycin (35.29 %), and a low incidence of resistance to gentamicin (6.53 %), kanamycin (8.49 %), chloramphenicol (9.15 %), and cefotaxime (10.45 %). The multiple antibiotic resistance index of each bacterial species indicated that bacteria from raised amphibians and reptiles have been exposed to tested antibiotics, with results ranging from 0 to 0.58. Most isolates showed tolerance to different concentrations of heavy metals, and minimal inhibition concentrations ranged from100 to >3,200 μg/mL. According to these results, a significant occurrence of bacteria in the internal organs of reptiles and amphibians, with a high incidence of resistance against antibiotics and heavy metals, may risk aquatic animals and the public health. These data appoint the importance of epidemiological surveillance and microbiological monitoring and reinforce the need to implement environment protection programs for amphibian and reptile species.
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References
Bauer, A. W., Kirby, W. M. M., Sherris, J. C., & Turck, M. (1966). Antibiotic susceptibility testing by a standardized single-disk method. American Journal of Clinical Pathology, 45, 493–496.
Bastos, H. M., Lopes, L. F. L., Gattamorta, M. A., & Matushima, E. R. (2008). Prevalence of Enterobacteriaceae in Bothrops jararaca in São Paulo State: microbiological survey and antimicrobial resistance standards. Acta Scientarum - Biological Science, 30(3), 321–326.
Clinical and Laboratory Standard Institute (CLSI). (2009). Performance standards for antimicrobial disk susceptibility tests. NCCLS Document M2-A7. National Committee for Clinical Laboratory Standards, 27(1), Wayne.
Ferronato, B. O., Marques, T. S., Souza, F. L., Verdade, L. M., & Matushima, E. R. (2009). Oral bacterial microbiota and traumatic injuries of free-ranging Phrynops geoffroanus (Testudines, Chelidae) in southeastern Brazil. Phllomedusa, 8(1), 19–25.
Filippi, E., D’Alterio, G. L., Brozzi, A. B., Micci, M., Politi, P., & Mantero, D. (2010). Note on the intestinal bacterial populations of free-living snakes in Italy. Herpetology Notes, 3, 263–265.
Kaoud, H. A., & Eldahshan, A. R. (2010). Bioaccumulation of cadmium in the freshwater prawn Macrobrachium rosenbergii. Nature and Science, 8(4), 157–168.
Hacioglu, N., & Dulger, B. (2011). Occurrence and antibiotic susceptibility of some bacteria in Saricay stream (Canakkale, Turkey). European Journal of Experimental Biology, 1(4), 158–163.
Hacioglu, N., Dulger, B., Caprazli, T., & Tosunoglu, M. (2011). A Study on microflora in oral and cloaca of freshwater turtles (Emys orbicularis Linnaeus, 1758 – Mauremys rivulata Valenciennes, 1833) from Kavak Delta (Canakkale). Paper presented at the VI. International Symposium on Ecology and Environmental Problems, Antalya – Turkey, 17–20 November 2011
Kelkit, A., Akbulak, C., Erginal, A. E., & Ozcan, H. (2008). Tourism activities in wetlands: a case study of Kavak Delta (Canakkale, NW Turkey). Ohrid, Republic of Macedonia: Proceedings of the conference on water observation and information system for decision support.
Krumpermann, P. H. (1983). Multiple antibiotic resistance indexing of E. coli to identify high-risk sources of fecal contamination of foods. Applied and Environmental Microbiology, 46(1), 165–170.
Lee, S. W., Najiah, M., Wendy, W., Nadirah, M., & Faizah, S. H. (2009). Occurence of heavy metals and antibiotic resistance in bacteria from intestinal organs of American bullfrog (Rana catesbeiana) raised in Malaysia. Journal of Venomous Animals and Toxins including Tropical Diseases, 15(2), 353–358.
Matyar, F., Kaya, A., & Dincer, S. (2008). Antibacterial agents and heavy metal resistance in gram-negative bacteria isolated from seawater, shrimp, and sediment in Iskenderun Bay, Turkey. Science of the Total Environment, 407, 279–285.
Murray, P. R., Baron, E. J., Pfaller, M. A., Tenover, F. C., & Yolken, R. H. (1999). Manual of clinical microbiology (7th ed.). Washington, D.C.: American Society for Microbiology.
Najiah, M., Lee, S. W., Wendy, W., Tee, L. W., Nadirah, M., & Faizah, S. H. (2009). Antibiotic resistance and heavy metals tolerance in gram-negative bacteria from diseased American Bullfrog (Rana catesbeiana) cultured in Malaysia. Agricultural Sciences in China, 8(10), 1270–1275.
Nies, D. H. (1999). Microbial heavy metal resistance. Applied Microbiology and Biotechnology, 51, 730–750.
Ogbondeminu, F. S. (1993). The occurrence and distribution of enteric bacteria in fish and water of tropical ponds in Nigeria. Journal of Aquaculture in the Tropics, 8, 61–66.
Ozcan, M., Kılıc, A., Kan, N. I., & Sarıeyyupoglu, M. (2006). A study on aerob bacteria in liver, spleen, kidney, and intestine of freshwater turtle (Mauremys caspica caspica Gmelin, 1774). Dogu Anadolu Bolgesi Arastirmalari, (DAUM), 5(1), 19–22.
Santoro, M., Hernandez, G., Caballero, M., & Garcia, F. (2006). Aerobic bacterial flora of nesting fren turtles (Chelonia mydas) from Tortuguero National Park, Costa Rica. Journal of Zoo and Wildlife Medicine, 37(4), 549–552.
Spain, A., & Alm, E. (2003). Implications of microbial heavy metal tolerance in the environment. Reviews in Undergraduate Research, 2, 1–6.
Soccini, C., & Ferri, V. (2004). Bacteriological of Trachemys scripta elegans and Emys orbicularis in the pop plain (Italy). Biologia, Bratislava, 59/Suppl, 14, 201–207.
Tee, L. W., & Najiah, M. (2011). Antibiogram and heavy metal tolerance of Bullfrog bacteria in Malaysia. Open Veterinary Journal, 1, 39–45.
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Hacioglu, N., Tosunoglu, M. Determination of antimicrobial and heavy metal resistance profiles of some bacteria isolated from aquatic amphibian and reptile species. Environ Monit Assess 186, 407–413 (2014). https://doi.org/10.1007/s10661-013-3385-y
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DOI: https://doi.org/10.1007/s10661-013-3385-y