Redirecting to http://dergipark.org.tr/_fragment?_hash=Zt4anftdf4-9WM68_DYATyu5KEn8voXzlOOQIMQD280&_path=id%3D1576629%26_format%3Dhtml%26_locale%3Den%26_controller%3DApp%255CController%255CSite%255CArticleController%253A%253AesiArticleStats.
Research Article
BibTex RIS Cite

The Relationship between Copper Tolerance and Antibiotic Susceptibility of Vagococcus salmoninarum Isolated from Kılavuzlu Dam Lake

Year 2025, Volume: 11 Issue: 1, 33 - 37, 30.04.2025

Hacı Bayram Gökhan , Ünal İspir , Mikail Özcan , Engin Şeker

https://doi.org/10.17216/limnofish.1576629

Abstract

The contamination of aquatic ecosystems by heavy metals has been identified as a significant environmental hazard for aquatic animal species, including fish. The objective of this study was to investigate the tolerance of Vagococcus salmoninarum bacteria to copper and the impact of copper exposure on antibiotic susceptibility. The bacterial isolates, comprising six strains, were obtained from rainbow trout reared in cage culture at Kılavuzlu Dam Lake. The initial assessment of antibiotic susceptibility was conducted using the Kirby-Bauer disc diffusion method, which was subsequently validated through the determination of minimum inhibitory concentration (MIC). The broth microdilution method was employed, with the bacterial isolates exposed to concentrations of copper sulphate ranging from 0.1 to 1 mM. The resistance to multiple antibiotics was altered to be significantly altered following exposure to copper sulphate. The minimum inhibitory concentration (MIC) value of copper was observed to be 0.4 mM against V. salmoninarum. It was noted that V. salmoninarum, which has been exposed to copper in its natural environment, has developed the capacity to withstand stress and has undergone a change in its physiological status.

Keywords

Bacteria Vagococcus salmoninarum antibiotic resistance antibiotic susceptibility copper

Ethical Statement

All animal studies were approved by the Animal Ethics Committee of KSÜZİRHADYEK and Research Institute (Protocol number: 2013/5-1).

Supporting Institution

Kahramanmaraş Sütçü Imam University

Thanks

Kahramanmaraş Sütçü Imam University, Agriculture Faculty,

References

  • Austin B, Austin DA. 2016. Bacterial Fish Pathogens; Diseases of Farmed and Wild Fish. Switzerland: Springer Cham 732 p.
  • Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV. 2006. Co-selection of Antibiotic and Metal Resistance. Trends Microbiol. 14(4):176-82. doi: 10.1016/j.tim.2006.02.006
  • Calomiris JJ, Armstrong JL, Seidler RJ. 1984. Association of Metal Tolerance with Multiple Antibiotic Resistance of Bacteria Isolated from Drinking Water. Appl Environ Microb. 47(6):1238-1242. doi: 10.1128/aem.47.6.1238-1242.1984
  • CLSI 2011. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-first Informational Supplement M100-S21. Wayne, PA, the USA: Clinical and Laboratory Standards Institute 165 p.
  • Daly JG. 1999. Other Bacterial Pathogens. In: Woo PTK, Bruno DW, editors. Fish Diseases and Disorders: Viral, Bacterial and Fungal Infections. New York: CAB International. p. 577-584.
  • Dang H, Song L, Chen M, Chang Y. 2006. Concurrence of cat and tet Genes in Multiple Antibiotic-Resistant Bacteria Isolated from a Sea Cucumber and sea Urchin Mariculture Farm in China. Microb Ecol. 52(4):634-643. doi: 10.1007/s00248-006-9091-3
  • Didinen BI, Kubilay A, Diler O, Ekici S, Onuk EE. Findik A. 2011. First Isolation of Vagococcus salmoninarum from Cultured Rainbow Trout (Oncorhynchus mykiss, Walbaum) broodstocks in Turkey. Bull Eur Ass Fish Pathol. 31(6):235-243.
  • Garhwal D, Vaghela G, Panwala T, Revdiwala S, Shah A, Mulla S. 2014. Lead Tolerance Capacity of Clinical Bacterial Isolates and Change in their Antibiotic Susceptibility Pattern after Exposure to a Heavy Metal. International Journal of Medicine and Public Health. 4(3):253-256. doi: 10.4103/2230-8598.137711
  • Ghittino C, Agnetti F, Panzieri C, Cabra S, Colussi S, Prearo M. 2004. L’ infezione da Vagococcus salmoninarum della trota iridea in Italia. Ittiopatol. 1:25-33. [in Italian]
  • Kimiran-Erdem A, Arslan-Aydogdu EO, Gurun S, Altun O. 2015. Determination of Multiple Antibiotic and Heavy Metal Resistance of the Bacteria Isolated from the Küçükçekmece Lagoon, Turkey. Pol J Environ Stud. 24(3):1077-1084. doi: 10.15244/pjoes/29202
  • Levy SB. 2001. Antibiotic Resistance: Consequences of Inaction. Clin Infect Dis. 33(Supplement_3):124-129. doi: 10.1086/321837
  • McArthur JV, Tuckfield RC. 2000. Spatial Patterns in Antibiotic Resistance among Stream Bacteria: Effects of Industrial Pollution. Appl Environ Microb. 66(9):3722-3726. doi: 10.1128/AEM.66.9.3722-3726.2000
  • Michel C, Nougayrede P, Eldar A, Sochon E, de Kinkelin P. 1997. Vagococcus salmoninarum, a Bacterium of Pathological Significance in Rainbow Trout Oncorhynchus mykiss Farming. Dis Aquat Organ. 30(3):199-208. doi:10.3354/dao030199
  • Michels HT, Wilks SA, Noyce JO, Keevil CW. 2005. Copper Alloys for Human Infectious Disease Control. Paper presented at: Materials Science and Technology Conference; Pittsburgh, the USA.
  • Nakahara H, Ishikawa T, Sarai Y, Kondo I, Mitsuhashi S. 1977. Frequency of Heavy-Metal Resistance in Bacteria from Inpatients in Japan. Nature 266(5598):165-167. doi: 10.1038/266165a0
  • Nies DH. 1999. Microbial Heavy-Metal Resistance. Appl Microbiol Biot. 51:730-750. doi: 10.1007/s002530051457
  • Nougayrède P, Michel C, Sochon E, Vuillaume A, de Kinkelin P. 1995. Vagococcosis, an Emerging Threat for Farmed Salmonid Populations. Paper presented at: 7th International Conference on Diseases of Fish and Shellfish; Palma de Mallorca, Spain.
  • Özcan M. Barış Y. 2019. Investigation of phenotypic and genotypic characteristics of isolation of strains Vagococcus salmoninarum cage business rainbow trouts (Oncorhynchus mykiss) of Kahramanmaras province (Turkey). J. of Ani. and Vet. Adv. 18(4):124-131 doi: 10.36478/javaa.2019.124.131.
  • Özcan M. İspir U. Yılmaz Y. 2016. Experimental Vagococcus salmoninarum infection in Rainbow Trout (Oncorhynchus mkiss) by intraperitoneal injection. IOSR Journal of Agriculture and Veterinary Science (IOSR-JAVS) 9(12): 68-72.
  • Özcan M. Yılmaz Y. Donat E. Kılavuz D. 2014. A study of Vagococcus salmoninarum infection in some cultured Rainbow Trout in cages in the Mediterranean and Southeast Anatolia regions. Journal of Fisheries and Aquatic Sciences 29(1): 2130.
  • Roane TM. Kellogg ST. 1995. Characterization of Bacterial Communities in Heavy Metal Contaminated Soils. Can J Microbiol. 42(6):593-603. doi: 10.1139/m96-080
  • Ruiz-Zarzuela I, de Bias I, Gironés, O, Ghittino C, MúAzquiz JL. 2005. Isolation of Vagococcus salmoninarum in Rainbow Trout, Oncorhynchus mykiss (Walbaum), Broodstocks: Characterization of the Pathogen. Vet Res Commun. 29(7):553-562. doi: 10.1007/s11259-005-2493-8
  • Salogni C, Perantoni P, Pitozzi A, Loris G, Alborali GL. 2007. Vagococcus salmoninarum: descrizione di un focolaio di malattia in riproduttori di trota iridea (Oncorhynchus mykiss). Ittiopatol. 4:59-66. [in Italian]
  • Schmidtke LN, Carson J. 1994. Characteristics of Vagococcus salmoninarum Isolated from Diseased Salmonid Fish. J Appl Bacteriol. 77(2):229-236. doi: 10.1111/j.1365-2672.1994.tb03068.x
  • Schwarz S, Kehrenberg C, Doublet B, Cloeckaert A. 2004. Molecular Basis of Bacterial Resistance to Chloramphenicol and Florfenicol. FEMS Microbiol Rev. 28(5):519-542. doi: 10.1016/j.femsre.2004.04.001
  • Spain A, Alm E. 2003. Implications of Microbial Heavy Metal Tolerance in the Environment. Reviews in Undergraduate Research. 2:1-6.
  • Stepanauskas R, Glenn TC, Jagoe CH, Tuckfield RC, Lindell AH, King CJ, McArthur JV. 2006. Coselection for Microbial Resistance to Metals and Antibiotics in Freshwater Microcosms. Environ Microbiol. 8(9):1510-1514. doi: 10.1111/j.1462-2920.2006.01091.x
  • Tanrıkul T, Avsever ML, Onuk EE, Didinen BI. 2014. Vagococcus salmoninarum, a Causative Agent of Disease in Rainbow Trout (Oncorhynchus mykiss, Walbaum) Broodstocks in the Aegean Region of Turkey. Etlik Vet Mikrobiyol Derg. 25(1):11-16.
  • Wallbanks S, Martinez-Murcia AJ, Fryer JL, Phillips BA, Collins MD. 1990. 16S rRNA Sequence Determination for Members of the Genus Carnobacterium and Related Lactic Acid Bacteria and Description of Vagococcus salmoninarum sp. nov. Int J Syst Bacteriol. 40(3):224-230. doi: 10.1099/00207713-40-3-224
  • Zhou Y, Xu YB, Xu JX, Zhang XH, Xu SH, Du QP. 2015. Combined Toxic Effects of Heavy Metals and Antibiotics on a Pseudomonas fluorescens strain ZY2 Isolated from Swine Wastewater. Int J Mol Sci. 16(2):2839-2850. doi: 10.3390/ijms16022839

Kılavuzlu Baraj Gölü’ndeki Alabalık İşletmelerinden İzole Edilen Vagococcus salmoninarum’da Bakır Toleransı ve Antibiyotik Duyarlılığı Arasındaki İlişkinin İncelenmesi

Year 2025, Volume: 11 Issue: 1, 33 - 37, 30.04.2025

Hacı Bayram Gökhan , Ünal İspir , Mikail Özcan , Engin Şeker

https://doi.org/10.17216/limnofish.1576629

Abstract

Sucul ekosistemlerin ağır metallerle kirlenmesi, balıklar da dahil olmak üzere sucul hayvan türleri için önemli bir çevresel tehlike olarak tanımlanmıştır. Bu çalışmanın amacı Vagococcus salmoninarum bakterisinin bakıra toleransını ve bakıra maruz kalmanın antibiyotik duyarlılığı üzerindeki etkisini araştırmaktır. Altı suştan oluşan bakteri izolatları Kılavuzlu Baraj Gölü'nde kafes kültüründe yetiştirilen gökkuşağı alabalıklarından elde edilmiştir. Antibiyotik duyarlılığının ilk değerlendirmesi Kirby-Bauer disk difüzyon yöntemi kullanılarak yapılmış ve daha sonra minimum inhibitör konsantrasyon (MİK) değeri belirlenerek doğrulanmıştır. Bakteri izolatları 0,1 ila 1 mM arasında değişen bakır sülfat konsantrasyonlarına maruz bırakılarak et suyu mikrodilüsyon yöntemi kullanılmıştır. Bakır sülfata maruz kalmanın ardından çoklu antibiyotik direncinin önemli ölçüde değiştiği bulunmuştur. Bakırın minimum inhibitör konsantrasyon (MİK) değerinin V. salmoninarum'a karşı 0,4 mM olduğu gözlenmiştir. Doğal ortamında bakıra maruz kalan V. salmoninarum'un strese dayanma kapasitesi geliştirdiği ve fizyolojik durumunda bir değişiklik olduğu kaydedilmiştir.

Keywords

Bakteri Vagococcus salmoninarum antibiyotik duyarlılık antibiyotik direnç bakır

References

  • Austin B, Austin DA. 2016. Bacterial Fish Pathogens; Diseases of Farmed and Wild Fish. Switzerland: Springer Cham 732 p.
  • Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV. 2006. Co-selection of Antibiotic and Metal Resistance. Trends Microbiol. 14(4):176-82. doi: 10.1016/j.tim.2006.02.006
  • Calomiris JJ, Armstrong JL, Seidler RJ. 1984. Association of Metal Tolerance with Multiple Antibiotic Resistance of Bacteria Isolated from Drinking Water. Appl Environ Microb. 47(6):1238-1242. doi: 10.1128/aem.47.6.1238-1242.1984
  • CLSI 2011. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-first Informational Supplement M100-S21. Wayne, PA, the USA: Clinical and Laboratory Standards Institute 165 p.
  • Daly JG. 1999. Other Bacterial Pathogens. In: Woo PTK, Bruno DW, editors. Fish Diseases and Disorders: Viral, Bacterial and Fungal Infections. New York: CAB International. p. 577-584.
  • Dang H, Song L, Chen M, Chang Y. 2006. Concurrence of cat and tet Genes in Multiple Antibiotic-Resistant Bacteria Isolated from a Sea Cucumber and sea Urchin Mariculture Farm in China. Microb Ecol. 52(4):634-643. doi: 10.1007/s00248-006-9091-3
  • Didinen BI, Kubilay A, Diler O, Ekici S, Onuk EE. Findik A. 2011. First Isolation of Vagococcus salmoninarum from Cultured Rainbow Trout (Oncorhynchus mykiss, Walbaum) broodstocks in Turkey. Bull Eur Ass Fish Pathol. 31(6):235-243.
  • Garhwal D, Vaghela G, Panwala T, Revdiwala S, Shah A, Mulla S. 2014. Lead Tolerance Capacity of Clinical Bacterial Isolates and Change in their Antibiotic Susceptibility Pattern after Exposure to a Heavy Metal. International Journal of Medicine and Public Health. 4(3):253-256. doi: 10.4103/2230-8598.137711
  • Ghittino C, Agnetti F, Panzieri C, Cabra S, Colussi S, Prearo M. 2004. L’ infezione da Vagococcus salmoninarum della trota iridea in Italia. Ittiopatol. 1:25-33. [in Italian]
  • Kimiran-Erdem A, Arslan-Aydogdu EO, Gurun S, Altun O. 2015. Determination of Multiple Antibiotic and Heavy Metal Resistance of the Bacteria Isolated from the Küçükçekmece Lagoon, Turkey. Pol J Environ Stud. 24(3):1077-1084. doi: 10.15244/pjoes/29202
  • Levy SB. 2001. Antibiotic Resistance: Consequences of Inaction. Clin Infect Dis. 33(Supplement_3):124-129. doi: 10.1086/321837
  • McArthur JV, Tuckfield RC. 2000. Spatial Patterns in Antibiotic Resistance among Stream Bacteria: Effects of Industrial Pollution. Appl Environ Microb. 66(9):3722-3726. doi: 10.1128/AEM.66.9.3722-3726.2000
  • Michel C, Nougayrede P, Eldar A, Sochon E, de Kinkelin P. 1997. Vagococcus salmoninarum, a Bacterium of Pathological Significance in Rainbow Trout Oncorhynchus mykiss Farming. Dis Aquat Organ. 30(3):199-208. doi:10.3354/dao030199
  • Michels HT, Wilks SA, Noyce JO, Keevil CW. 2005. Copper Alloys for Human Infectious Disease Control. Paper presented at: Materials Science and Technology Conference; Pittsburgh, the USA.
  • Nakahara H, Ishikawa T, Sarai Y, Kondo I, Mitsuhashi S. 1977. Frequency of Heavy-Metal Resistance in Bacteria from Inpatients in Japan. Nature 266(5598):165-167. doi: 10.1038/266165a0
  • Nies DH. 1999. Microbial Heavy-Metal Resistance. Appl Microbiol Biot. 51:730-750. doi: 10.1007/s002530051457
  • Nougayrède P, Michel C, Sochon E, Vuillaume A, de Kinkelin P. 1995. Vagococcosis, an Emerging Threat for Farmed Salmonid Populations. Paper presented at: 7th International Conference on Diseases of Fish and Shellfish; Palma de Mallorca, Spain.
  • Özcan M. Barış Y. 2019. Investigation of phenotypic and genotypic characteristics of isolation of strains Vagococcus salmoninarum cage business rainbow trouts (Oncorhynchus mykiss) of Kahramanmaras province (Turkey). J. of Ani. and Vet. Adv. 18(4):124-131 doi: 10.36478/javaa.2019.124.131.
  • Özcan M. İspir U. Yılmaz Y. 2016. Experimental Vagococcus salmoninarum infection in Rainbow Trout (Oncorhynchus mkiss) by intraperitoneal injection. IOSR Journal of Agriculture and Veterinary Science (IOSR-JAVS) 9(12): 68-72.
  • Özcan M. Yılmaz Y. Donat E. Kılavuz D. 2014. A study of Vagococcus salmoninarum infection in some cultured Rainbow Trout in cages in the Mediterranean and Southeast Anatolia regions. Journal of Fisheries and Aquatic Sciences 29(1): 2130.
  • Roane TM. Kellogg ST. 1995. Characterization of Bacterial Communities in Heavy Metal Contaminated Soils. Can J Microbiol. 42(6):593-603. doi: 10.1139/m96-080
  • Ruiz-Zarzuela I, de Bias I, Gironés, O, Ghittino C, MúAzquiz JL. 2005. Isolation of Vagococcus salmoninarum in Rainbow Trout, Oncorhynchus mykiss (Walbaum), Broodstocks: Characterization of the Pathogen. Vet Res Commun. 29(7):553-562. doi: 10.1007/s11259-005-2493-8
  • Salogni C, Perantoni P, Pitozzi A, Loris G, Alborali GL. 2007. Vagococcus salmoninarum: descrizione di un focolaio di malattia in riproduttori di trota iridea (Oncorhynchus mykiss). Ittiopatol. 4:59-66. [in Italian]
  • Schmidtke LN, Carson J. 1994. Characteristics of Vagococcus salmoninarum Isolated from Diseased Salmonid Fish. J Appl Bacteriol. 77(2):229-236. doi: 10.1111/j.1365-2672.1994.tb03068.x
  • Schwarz S, Kehrenberg C, Doublet B, Cloeckaert A. 2004. Molecular Basis of Bacterial Resistance to Chloramphenicol and Florfenicol. FEMS Microbiol Rev. 28(5):519-542. doi: 10.1016/j.femsre.2004.04.001
  • Spain A, Alm E. 2003. Implications of Microbial Heavy Metal Tolerance in the Environment. Reviews in Undergraduate Research. 2:1-6.
  • Stepanauskas R, Glenn TC, Jagoe CH, Tuckfield RC, Lindell AH, King CJ, McArthur JV. 2006. Coselection for Microbial Resistance to Metals and Antibiotics in Freshwater Microcosms. Environ Microbiol. 8(9):1510-1514. doi: 10.1111/j.1462-2920.2006.01091.x
  • Tanrıkul T, Avsever ML, Onuk EE, Didinen BI. 2014. Vagococcus salmoninarum, a Causative Agent of Disease in Rainbow Trout (Oncorhynchus mykiss, Walbaum) Broodstocks in the Aegean Region of Turkey. Etlik Vet Mikrobiyol Derg. 25(1):11-16.
  • Wallbanks S, Martinez-Murcia AJ, Fryer JL, Phillips BA, Collins MD. 1990. 16S rRNA Sequence Determination for Members of the Genus Carnobacterium and Related Lactic Acid Bacteria and Description of Vagococcus salmoninarum sp. nov. Int J Syst Bacteriol. 40(3):224-230. doi: 10.1099/00207713-40-3-224
  • Zhou Y, Xu YB, Xu JX, Zhang XH, Xu SH, Du QP. 2015. Combined Toxic Effects of Heavy Metals and Antibiotics on a Pseudomonas fluorescens strain ZY2 Isolated from Swine Wastewater. Int J Mol Sci. 16(2):2839-2850. doi: 10.3390/ijms16022839
There are 30 citations in total.

Details

Primary Language English
Subjects Aquaculture and Fisheries (Other)
Journal Section Research Article
Authors

Hacı Bayram Gökhan 0000-0001-8094-5546

Ünal İspir 0000-0002-2077-0219

Mikail Özcan 0000-0001-9032-0697

Engin Şeker 0000-0003-2906-6006

Early Pub Date April 28, 2025
Publication Date April 30, 2025
Submission Date October 31, 2024
Acceptance Date January 21, 2025
Published in Issue Year 2025 Volume: 11 Issue: 1

Cite

APA Gökhan, H. B., İspir, Ü., Özcan, M., Şeker, E. (2025). The Relationship between Copper Tolerance and Antibiotic Susceptibility of Vagococcus salmoninarum Isolated from Kılavuzlu Dam Lake. Journal of Limnology and Freshwater Fisheries Research, 11(1), 33-37. https://doi.org/10.17216/limnofish.1576629
 Download Cover Image