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Investigation of multiple resistance frequencies (antibiotic and heavy metal) of bacteria isolated from Gökçeada Island coastal marine sediment

Year 2025, Volume: 8 Issue: 1, 1 - 11

Pelin Saliha Çiftçi Türetken , Samet Kalkan , Gülşen Altuğ

Abstract

Marine sediments are important reservoirs for antibiotics and heavy metals. Bacteria play a key role in polluted sedimentary habitats. This study aimed to identify heavy metal and antibiotic resistance in marine sediment bacteria isolated from Gökçeada Island in Turkiye. The samples were collected seasonally from 10 different sampling stations in 2015. Ninety isolates determined by VITEK 2 were tested against seven antibiotics using the disk diffusion method. The minimum inhibitory concentration values were measured against four heavy metal salts. The antibiotic resistance frequency rates were ordered as sulphonamides compound (93.3%), cefotaxime (78.9), ampicillin (77.8%), oxacillin (67.8%), rifampicin (57.8%), imipenem (1.1%), and oxytetracycline (0%). The heavy metal resistance ratios against ZnCl2, CuSO4, Pb(CH3COO)2, and HgCl2 were measured as 100%, 100%, 96.7%, and 73.3% respectively. The multiple heavy metal resistance index values were ranged from 0.75 (22.2%) to 1.0 (77.8%). The results show significant heavy metal and antibiotic contamination in the sediments of the Gökçeada Island. It is recommended that measures be taken against antibiotics and heavy metal pollution, as well as identifying and monitoring critical control points.

Keywords

Antibiotic resistance Gökçeada island Heavy metal resistance Heterotrophic bacteria Marine sediment

Project Number

Istanbul University Scientific Research Projects Unit (Project number: 50725)

References

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  • Acarli, D., Kale, S., & Çakır, K. (2018). A new maximum length for the garfish, Belone belone (Linnaeus, 1761) in the coast of Gökçeada Island (Aegean Sea. Turkiye). Cahiers de Biologie Marine, 59(4), 385-389. https://doi.org/10.21411/CBM.A.55A28635
  • Akmirza, A. (2013). Monogeneans of fish near Gökçeada, Turkiye. Turkish Journal of Zoology, 37(4), 441-448. https://doi.org/10.3906/zoo-1205-4
  • Altın, A., & Ayyıldız, H. (2018). Relationships between total length and otolith measurements for 36 fish species from Gökçeada Island, Turkiye. Journal of Applied Ichthyology, 34(1), 136-141. https://doi.org/10.1111/jai.13509
  • Altuğ, G., & Balkıs, N. (2009). Levels of some toxic elements and frequency of bacterial heavy metal resistance in sediment and sea water. Environmental Monitoring and Assessment, 149(1), 61-69. https://doi.org/10.1007/s10661-008-0183-z
  • Altug, G., Cardak, M., Gurun, S., Ciftci, P. S., Saad, A., Ibrahim, A., & Fakhri, M. (2010). Biodiversity of Culturable Aerobic Heterotrophic Bacteria in the Coastal Areas of Syria, Lebanon and the Offshore Area in the Northern Aegean Sea. In The International Conference on Biodiversity of the Aquatic Environment: Towards a Diverse and Sustainable World, Syria (pp. 115-125).
  • Altuğ, G., Çardak, M., Türetken, P.S.Ç., Kalkan, S., & Gürün, S. (2020). Antibiotic and heavy metal resistant bacteria isolated from Aegean Sea water and sediment in Güllük Bay, Turkiye. Johnson Matthey Technology Review. https://doi.org/10.1595/205651320x15953337767424
  • Arndt, S., Jørgensen, B.B., LaRowe, D.E., Middelburg, J.J., Pancost, R.D., & Regnier, P. (2013). Quantifying the degradation of organic matter in marine sediments: A review and synthesis. Earth-Science Reviews, 123, 53-86. https://doi.org/10.1016/j.earscirev.2013.02.008
  • Aslan, H., Elipek, B., Gönülal, O., Baytut, Ö., Kurt, Y., & İnanmaz, Ö.E. (2021). Gökçeada Salt Lake: A case study of seasonal dynamics of wetland ecological communities in the context of anthropogenic pressure and nature conservation. Wetlands, 41(2), 1-14. https://doi.org/10.1007/s13157-021-01401-0
  • Baker-Austin, C., Wright, M.S., Stepanauskas, R., & McArthur, J.V. (2006). Co-selection of antibiotic and metal resistance. Trends in Microbiology, 14(4), 176-182. https://doi.org/10.1016/j.tim.2006.02.006
  • Balkıs, H., Balkıs, N., & Altınsaçlı, S. (2001). The crab species found on the coasts of Gökçeada (Imbroz) Island in the Aegean Sea. Hydrobiologia, 449(1), 99-103. https://doi.org/10.1023/A:1017593003458
  • Baquero, F., Martínez, J.L., & Cantón, R. (2008). Antibiotics and antibiotic resistance in water environments. Current Opinion in Biotechnology, 19(3), 260-265. https://doi.org/10.1016/j.copbio.2008.05.006
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  • Cardak, M., Altug, G., & Türetken, P.S.C. (2013). Rapports et procès-verbaux des réunions Commission internationale pour l'exploration scientifique de la Mer Méditerranée 40(407), Marseille France.
  • Çardak, M., Altug, G., Ay, M., & Erol, Ô. (2016). Distribution of antibiotic resistance and the presence of vancomycin-resistance genes (vanA and vanB) in Enterobacteriaceae isolated from the Sea of Marmara, the Canakkale Strait and the Istanbul Strait, Turkiye. Oceanological and Hydrobiological Studies, 45(2), https://doi.org/182-190. 10.1515/ohs-2016-0017
  • Çiftçi-Türetken, P.S., & Altuğ, G. (2013). Seasonal variations of the levels of total and culturable heterotrophic bacteria around Gökçeada Island (The Northern Aegean Sea), Turkiye. Rapports et procès-verbaux des réunions Commission internationale pour l'exploration scientifique de la Mer Méditerranée, 40, Marseille France.
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  • Dell'Anno, A., Mei, M.L., Ianni, C., & Danovaro, R. (2003). Impact of bioavailable heavy metals on bacterial activities in coastal marine sediments. World Journal of Microbiology and Biotechnology, 19(1), 93-100. https://doi.org/10.1023/A:1022581632116
  • Gillan, D.C., Danis, B., Pernet, P., Joly, G., & Dubois, P. (2005). Structure of sediment-associated microbial communities along a heavy-metal contamination gradient in the marine environment. Applied and Environmental Microbiology, 71(2), 679-690. https://doi.org/10.1128/AEM.71.2.679-690.2005
  • Gillard, B., Chatzievangelou, D., Thomsen, L., Ullrich, M.S. (2019). Heavy-metal-resistant microorganisms in deep-sea sediments disturbed by mining activity: An application towards the development of an experimental in vitro systems. Frontiers in Marine Science, 6, 462. https://doi.org/10.3389/fmars.2019.00462
  • Gönülal, O., & Güreşen, S.O. (2014). A list of macrofauna on the continental shelf of Gökçeada Island (northern Aegean Sea) with a new record (Gryphus vitreus Born, 1778) (Brachiopoda, Rhynchonellata) for the Turkish seas. Journal of the Black Sea/Mediterranean Environment, 20(3), 228-252.
  • Güreşen, A., Güreşen, S.O., & Aktan, Y. (2020). Temporal and bathymetric variation of epiphytic microalgae on Posidonia oceanica (L.) delile leaves in Gökçeada (North Aegean, Turkiye). Turkish Journal of Fisheries and Aquatic Sciences, 20(10), 727-737. https://doi.org/10.4194/1303-2712-v20_10_02
  • Hoshino, T., Doi, H., Uramoto, G. I., Wörmer, L., Adhikari, R.R., Xiao, N., ... & Inagaki, F. (2020). Global diversity of microbial communities in marine sediment. Proceedings of the National Academy of Sciences, 117(44), 27587-27597. https://doi.org/10.1073/pnas.1919139117
  • Iyer, A., Mody, K., & Jha, B. (2005). Biosorption of heavy metals by a marine bacterium. Marine Pollution Bulletin, 50(3), 340-343. https://doi.org/10.1016/j.marpolbul.2004.11.012
  • Jørgensen, B.B., & Boetius, A. (2007). Feast and famine—microbial life in the deep-sea bed. Nature Reviews Microbiology, 5(10), 770-781. https://doi.org/10.1038/nrmicro1745
  • Kacar, A.S.L.I., & Kocyigit, A. (2013). Characterization of heavy metal and antibiotic resistant bacteria isolated from Aliaga Ship Dismantling Zone, Eastern Aegean Sea, Turkiye. International Journal of Environmental Research, 7(4), 895-902. https://doi.org/10.22059/IJER.2013.671
  • Kaçar, A., Koçyiğit, A., & Uluturhan, E. (2013). Heavy Metal Tolerance of Sediment Bacteria Isolated from Coastal City (Izmir, Turkiye). Rapports et procès-verbaux des réunions Commission internationale pour l'exploration scientifique de la Mer Méditerranée, 40(410), Marseille France.
  • Kahraman, A., Kaynak, G., Gurler, O. Yalcin, S., Ozturk, S., & Gundogdu, O. (2009). Investigation of environmental contamination in lichens of Gökçeada (Imbroz) Island in Turkiye. Radiation Measurements, 44(2), 199-202. https://doi.org/10.1016/j.radmeas.2009.01.006
  • Keskin, Ç., & Ünsal, N. (1998). The fish fauna of Gökçeada Island, NE Aegean Sea, Turkiye. Italian Journal of Zoology, 65(S1), 299-302. https://doi.org/10.1080/11250009809386836
  • Krumperman, P.H. (1983). Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Applied and environmental Microbiology, 46(1), 165-170. https://doi.org/10.1128/aem.46.1.165-170.1983
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  • Larsson, D.J. (2014). Antibiotics in the environment. Upsala Journal of Medical Sciences, 119(2), 108-112. https://doi.org/10.3109/03009734.2014.896438
  • Marti, E., Variatza, E., & Balcazar, J.L. (2014). The role of aquatic ecosystems as reservoirs of antibiotic resistance. Trends in Microbiology, 22(1), 36-41. https://doi.org/10.1016/j.tim.2013.11.001
  • Matyar, F. (2012). Antibiotic and heavy metal resistance in bacteria isolated from the eastern Mediterranean Sea coast”, Bull. Environ. Contam. Toxicol., 89, 551–556. https://doi.org/10.1007/s00128-012-0726-4
  • Matyar, F., Kaya, A., & Dinçer, S. (2008). Antibacterial agents and heavy metal resistance in Gram-negative bacteria isolated from seawater, shrimp and sediment in Iskenderun Bay, Turkiye. Science of the Total Environment, 407(1), 279-285. https://doi.org/10.1016/j.scitotenv.2008.08.014
  • Näslund, J., Hedman, J.E., & Agestrand, C. (2008). Effects of the antibiotic ciprofloxacin on the bacterial community structure and degradation of pyrene in marine sediment. Aquatic Toxicology, 90(3), 223-227. https://doi.org/10.1016/j.aquatox.2008.09.002
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Year 2025, Volume: 8 Issue: 1, 1 - 11

Pelin Saliha Çiftçi Türetken , Samet Kalkan , Gülşen Altuğ

Abstract

Project Number

Istanbul University Scientific Research Projects Unit (Project number: 50725)

References

  • Ab Rahman, N., Chowdhury, A. J. K., & Abidin, Z. A. Z. (2015). Antibiotic resistant bacteria from sediment of coastal water of Pahang, Malaysia. Jurnal Teknologi, 77(24). https://doi.org/10.11113/jt.v77.6709
  • Acarli, D., Kale, S., & Çakır, K. (2018). A new maximum length for the garfish, Belone belone (Linnaeus, 1761) in the coast of Gökçeada Island (Aegean Sea. Turkiye). Cahiers de Biologie Marine, 59(4), 385-389. https://doi.org/10.21411/CBM.A.55A28635
  • Akmirza, A. (2013). Monogeneans of fish near Gökçeada, Turkiye. Turkish Journal of Zoology, 37(4), 441-448. https://doi.org/10.3906/zoo-1205-4
  • Altın, A., & Ayyıldız, H. (2018). Relationships between total length and otolith measurements for 36 fish species from Gökçeada Island, Turkiye. Journal of Applied Ichthyology, 34(1), 136-141. https://doi.org/10.1111/jai.13509
  • Altuğ, G., & Balkıs, N. (2009). Levels of some toxic elements and frequency of bacterial heavy metal resistance in sediment and sea water. Environmental Monitoring and Assessment, 149(1), 61-69. https://doi.org/10.1007/s10661-008-0183-z
  • Altug, G., Cardak, M., Gurun, S., Ciftci, P. S., Saad, A., Ibrahim, A., & Fakhri, M. (2010). Biodiversity of Culturable Aerobic Heterotrophic Bacteria in the Coastal Areas of Syria, Lebanon and the Offshore Area in the Northern Aegean Sea. In The International Conference on Biodiversity of the Aquatic Environment: Towards a Diverse and Sustainable World, Syria (pp. 115-125).
  • Altuğ, G., Çardak, M., Türetken, P.S.Ç., Kalkan, S., & Gürün, S. (2020). Antibiotic and heavy metal resistant bacteria isolated from Aegean Sea water and sediment in Güllük Bay, Turkiye. Johnson Matthey Technology Review. https://doi.org/10.1595/205651320x15953337767424
  • Arndt, S., Jørgensen, B.B., LaRowe, D.E., Middelburg, J.J., Pancost, R.D., & Regnier, P. (2013). Quantifying the degradation of organic matter in marine sediments: A review and synthesis. Earth-Science Reviews, 123, 53-86. https://doi.org/10.1016/j.earscirev.2013.02.008
  • Aslan, H., Elipek, B., Gönülal, O., Baytut, Ö., Kurt, Y., & İnanmaz, Ö.E. (2021). Gökçeada Salt Lake: A case study of seasonal dynamics of wetland ecological communities in the context of anthropogenic pressure and nature conservation. Wetlands, 41(2), 1-14. https://doi.org/10.1007/s13157-021-01401-0
  • Baker-Austin, C., Wright, M.S., Stepanauskas, R., & McArthur, J.V. (2006). Co-selection of antibiotic and metal resistance. Trends in Microbiology, 14(4), 176-182. https://doi.org/10.1016/j.tim.2006.02.006
  • Balkıs, H., Balkıs, N., & Altınsaçlı, S. (2001). The crab species found on the coasts of Gökçeada (Imbroz) Island in the Aegean Sea. Hydrobiologia, 449(1), 99-103. https://doi.org/10.1023/A:1017593003458
  • Baquero, F., Martínez, J.L., & Cantón, R. (2008). Antibiotics and antibiotic resistance in water environments. Current Opinion in Biotechnology, 19(3), 260-265. https://doi.org/10.1016/j.copbio.2008.05.006
  • Bauer, A.T. (1966). Antibiotic susceptibility testing by a standardized single disc method. American Journal of Clinical Pathology, 45, 149-158.
  • Belivermiş, M., Kılıç, Ö., Efe, E., Sezer, N., Gönülal, O., & Kaya, T.N.A. (2019). Mercury and Po-210 in mollusc species in the island of Gökçeada in the north-eastern Aegean Sea: Bioaccumulation and risk assessment for human consumers. Chemosphere, 235, 876-884. https://doi.org/ 10.1016/j.chemosphere.2019.06.214
  • Bryan, G.W., & Langston, W.J. (1992). Bioavailability, accumulation and effects of heavy metals in sediments with special reference to United Kingdom estuaries: A review. Environmental Pollution, 76(2), 89-131. https://doi.org/10.1016/0269-7491(92)90099-V
  • Buccolieri, A., Buccolieri, G., Cardellicchio, N., Dell'Atti, A., Di Leo, A., & Maci, A. (2006). Heavy metals in marine sediments of Taranto Gulf (Ionian Sea, southern Italy). Marine Chemistry, 99(1-4), 227-235. https://doi.org/10.1016/j.marchem.2005.09.009
  • Cardak, M., Altug, G., & Türetken, P.S.C. (2013). Rapports et procès-verbaux des réunions Commission internationale pour l'exploration scientifique de la Mer Méditerranée 40(407), Marseille France.
  • Çardak, M., Altug, G., Ay, M., & Erol, Ô. (2016). Distribution of antibiotic resistance and the presence of vancomycin-resistance genes (vanA and vanB) in Enterobacteriaceae isolated from the Sea of Marmara, the Canakkale Strait and the Istanbul Strait, Turkiye. Oceanological and Hydrobiological Studies, 45(2), https://doi.org/182-190. 10.1515/ohs-2016-0017
  • Çiftçi-Türetken, P.S., & Altuğ, G. (2013). Seasonal variations of the levels of total and culturable heterotrophic bacteria around Gökçeada Island (The Northern Aegean Sea), Turkiye. Rapports et procès-verbaux des réunions Commission internationale pour l'exploration scientifique de la Mer Méditerranée, 40, Marseille France.
  • Clinical and Laboratory Standards Institute (CLSI) (2018). Performance Standards for Antimicrobial Disk Susceptibility Tests. 13th ed. CLSI standard M02. Clinical and Laboratory Standards Institute. Wayne, PA.
  • Dell'Anno, A., Mei, M.L., Ianni, C., & Danovaro, R. (2003). Impact of bioavailable heavy metals on bacterial activities in coastal marine sediments. World Journal of Microbiology and Biotechnology, 19(1), 93-100. https://doi.org/10.1023/A:1022581632116
  • Gillan, D.C., Danis, B., Pernet, P., Joly, G., & Dubois, P. (2005). Structure of sediment-associated microbial communities along a heavy-metal contamination gradient in the marine environment. Applied and Environmental Microbiology, 71(2), 679-690. https://doi.org/10.1128/AEM.71.2.679-690.2005
  • Gillard, B., Chatzievangelou, D., Thomsen, L., Ullrich, M.S. (2019). Heavy-metal-resistant microorganisms in deep-sea sediments disturbed by mining activity: An application towards the development of an experimental in vitro systems. Frontiers in Marine Science, 6, 462. https://doi.org/10.3389/fmars.2019.00462
  • Gönülal, O., & Güreşen, S.O. (2014). A list of macrofauna on the continental shelf of Gökçeada Island (northern Aegean Sea) with a new record (Gryphus vitreus Born, 1778) (Brachiopoda, Rhynchonellata) for the Turkish seas. Journal of the Black Sea/Mediterranean Environment, 20(3), 228-252.
  • Güreşen, A., Güreşen, S.O., & Aktan, Y. (2020). Temporal and bathymetric variation of epiphytic microalgae on Posidonia oceanica (L.) delile leaves in Gökçeada (North Aegean, Turkiye). Turkish Journal of Fisheries and Aquatic Sciences, 20(10), 727-737. https://doi.org/10.4194/1303-2712-v20_10_02
  • Hoshino, T., Doi, H., Uramoto, G. I., Wörmer, L., Adhikari, R.R., Xiao, N., ... & Inagaki, F. (2020). Global diversity of microbial communities in marine sediment. Proceedings of the National Academy of Sciences, 117(44), 27587-27597. https://doi.org/10.1073/pnas.1919139117
  • Iyer, A., Mody, K., & Jha, B. (2005). Biosorption of heavy metals by a marine bacterium. Marine Pollution Bulletin, 50(3), 340-343. https://doi.org/10.1016/j.marpolbul.2004.11.012
  • Jørgensen, B.B., & Boetius, A. (2007). Feast and famine—microbial life in the deep-sea bed. Nature Reviews Microbiology, 5(10), 770-781. https://doi.org/10.1038/nrmicro1745
  • Kacar, A.S.L.I., & Kocyigit, A. (2013). Characterization of heavy metal and antibiotic resistant bacteria isolated from Aliaga Ship Dismantling Zone, Eastern Aegean Sea, Turkiye. International Journal of Environmental Research, 7(4), 895-902. https://doi.org/10.22059/IJER.2013.671
  • Kaçar, A., Koçyiğit, A., & Uluturhan, E. (2013). Heavy Metal Tolerance of Sediment Bacteria Isolated from Coastal City (Izmir, Turkiye). Rapports et procès-verbaux des réunions Commission internationale pour l'exploration scientifique de la Mer Méditerranée, 40(410), Marseille France.
  • Kahraman, A., Kaynak, G., Gurler, O. Yalcin, S., Ozturk, S., & Gundogdu, O. (2009). Investigation of environmental contamination in lichens of Gökçeada (Imbroz) Island in Turkiye. Radiation Measurements, 44(2), 199-202. https://doi.org/10.1016/j.radmeas.2009.01.006
  • Keskin, Ç., & Ünsal, N. (1998). The fish fauna of Gökçeada Island, NE Aegean Sea, Turkiye. Italian Journal of Zoology, 65(S1), 299-302. https://doi.org/10.1080/11250009809386836
  • Krumperman, P.H. (1983). Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Applied and environmental Microbiology, 46(1), 165-170. https://doi.org/10.1128/aem.46.1.165-170.1983
  • Kümmerer, K. (2009). Antibiotics in the aquatic environment–a review–part II. Chemosphere, 75(4), 435-441. https://doi.org/10.1016/j.chemosphere.2008.11.086
  • Larsson, D.J. (2014). Antibiotics in the environment. Upsala Journal of Medical Sciences, 119(2), 108-112. https://doi.org/10.3109/03009734.2014.896438
  • Marti, E., Variatza, E., & Balcazar, J.L. (2014). The role of aquatic ecosystems as reservoirs of antibiotic resistance. Trends in Microbiology, 22(1), 36-41. https://doi.org/10.1016/j.tim.2013.11.001
  • Matyar, F. (2012). Antibiotic and heavy metal resistance in bacteria isolated from the eastern Mediterranean Sea coast”, Bull. Environ. Contam. Toxicol., 89, 551–556. https://doi.org/10.1007/s00128-012-0726-4
  • Matyar, F., Kaya, A., & Dinçer, S. (2008). Antibacterial agents and heavy metal resistance in Gram-negative bacteria isolated from seawater, shrimp and sediment in Iskenderun Bay, Turkiye. Science of the Total Environment, 407(1), 279-285. https://doi.org/10.1016/j.scitotenv.2008.08.014
  • Näslund, J., Hedman, J.E., & Agestrand, C. (2008). Effects of the antibiotic ciprofloxacin on the bacterial community structure and degradation of pyrene in marine sediment. Aquatic Toxicology, 90(3), 223-227. https://doi.org/10.1016/j.aquatox.2008.09.002
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There are 49 citations in total.

Details

Primary Language English
Subjects Hydrobiology
Journal Section Research Articles
Authors

Pelin Saliha Çiftçi Türetken 0000-0002-4377-1628

Samet Kalkan 0000-0002-5110-5609

Gülşen Altuğ 0000-0003-3251-7699

Project Number Istanbul University Scientific Research Projects Unit (Project number: 50725)
Early Pub Date November 2, 2024
Publication Date
Submission Date February 21, 2024
Acceptance Date May 30, 2024
Published in Issue Year 2025Volume: 8 Issue: 1

Cite

APA Çiftçi Türetken, P. S., Kalkan, S., & Altuğ, G. (2024). Investigation of multiple resistance frequencies (antibiotic and heavy metal) of bacteria isolated from Gökçeada Island coastal marine sediment. Aquatic Research, 8(1), 1-11.
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