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Cu, Cd, As and Hg resistance levels in Escherichia coli isolated from Mediterranean mussel and sea snail in the Southeastern Black Sea

Yıl 2021, Cilt: 10 Sayı: 1, 36 - 41, 31.03.2021
https://doi.org/10.33714/masteb.776902

Öz

Marine environment is exposed to various pollutants such as heavy metals, pesticides, and antibiotics. Bacterial resistance to these pollutants is a global problem all over the world. In this study, Mediterranean mussel (Mytilus galloprovincialis) and sea snail (Rapana venosa) were collected from 12 sampling points from Artvin, Rize, Trabzon, and Giresun Coasts of Black Sea, Turkey. A total of 54 Escherichia coli isolated from Mediterranean mussel and sea snail were tested for their ability to tolerate Cu, Cd, As, and Hg. For this purpose, minimum inhibitory concentration (MIC) tests for all isolates to the Cu, Cd, As, and Hg were done to determine tolerance or resistance using the broth dilution technique. MIC concentration for Cu, Cd, As, and Hg ranged between 100-400 μg/ml, 100-200 μg/ml, 25-400 μg/ml, and 3.125-25 μg/ml, respectively. All of the strains were determined as resistant to Cu, but sensitive to As. Resistance to Hg was determined as 7.4 %. The most common resistance gene in the bacteria was nccA and followed by chrB and merA. Tolerance or resistance of the bacteria to toxic pollutants including heavy metal(oid)s is of significant ecological importance. These bacteria could be used for monitoring environmental heavy metal(oid) pollution.

Destekleyen Kurum

Recep Tayyip Erdoğan University

Proje Numarası

2015.53006.103.02.04

Teşekkür

A part of this study was supported by Recep Tayyip Erdogan University Scientific Research Project Fund (Project No: 2015.53006.103.02.04). We would like to thank the anonymous reviewers for their comments. This study was presented in abstract form as an oral presentation to the International Congress on Engineering and Life Sciences (ICELIS-2018), Kastamonu, Turkey, 26–29 April 2018.

Kaynakça

  • Abou-Shanab, R. A. I., van Berkum, P. & Angle, J. S. (2007). Heavy metal resistance and genotypic analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale. Chemosphere, 68(2): 360-367. https://doi.org/10.1016/j.chemosphere.2006. 12.051
  • Abskharon, R. N. N., Hassan, S. H. A., Gad El-Rab, S. M. F. & Shoreit, A. A. M. (2008). Heavy metal resistant of E. coli isolated from wastewater sites in Assiut City, Egypt. Bulletin of Environmental Contamination and Toxicology, 81(3): 309. https://doi.org/10.1007/s00128-008-9494-6
  • Akçay, M. & Moon, C. J. (2004). The environmental impact of mining in the Pontides, Turkey: Reconnaissance sampling and GIS-based analysis. Geochemistry: Exploration, Environment, Analysis, 4(4): 317-328. https://doi.org/10.1144/1467-7873/03-052
  • Akinbowale, O. L., Peng, H., Grant, P. & Barton, M. D. (2007). Antibiotic and heavy metal resistance in motile aeromonads and pseudomonads from rainbow trout (Oncorhynchus mykiss) farms in Australia. International Journal of Antimicrobial Agents, 30(2): 177-182. https://doi.org/10.1016/j.ijantimicag.2007.03.012
  • Avşar, C. & Berber, İ. (2014). Plasmid profiling and antibiotics resistance of Escherichia coli strains isolated from Mytilus galloprovincialis and seawater. Journal of Coastal Life Medicine, 2(9): 689-693. https://doi.org/10.12980/JCLM.2.2014JCLM-2014-0069
  • Baltas, H., Sirin, M., Dalgic, G., Bayrak, E. Y. & Akdeniz, A. (2017). Assessment of metal concentrations (Cu, Zn, and Pb) in seawater, sediment and biota samples in the coastal area of Eastern Black Sea, Turkey. Marine Pollution Bulletin, 122(1-2): 475-482. https://doi.org/10.1016/j.marpolbul.2017.06.059
  • Bat, L. & Öztekin, H. C. (2016). Heavy metals in Mytilus galloprovincialis, Rapana venosa and Eriphia verrucosa from the Black Sea coasts of Turkey as bioindicators of pollution. Walailak Journal of Science and Technology, 13(9): 715-728.
  • Boran, H., Terzi, E., Altinok, I., Capkin, E. & Bascinar, N. (2013). Bacterial diseases of cultured Mediterranean horse mackerel (Trachurus mediterraneus) in sea cages. Aquaculture, 396: 8-13. https://doi.org/10.1016/ j.aquaculture.2013.02.025
  • Capkin, E., Ozdemir, S., Ozturk, R. C. & Altinok, I. (2017). Determination and transferability of plasmid‐mediated antibiotic resistance genes of the bacteria isolated from rainbow trout. Aquaculture Research, 48(11): 5561-5575.
  • Capkin, E., Terzi, E. & Altinok, I. (2015). Occurrence of antibiotic resistance genes in culturable bacteria isolated from Turkish trout farms and their local aquatic environment. Diseases of Aquatic Organisms, 114(2): 127-137. https://doi.org/10.3354/dao02852
  • Chapman, J. S. (2003). Disinfectant resistance mechanisms, cross-resistance, and co-resistance. International Biodeterioration & Biodegradation, 51(4): 271-276. https://doi.org/10.1016/S0964-8305(03)00044-1
  • CLSI (Clinical and Laboratory Standards Institute). (2018). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, (11th Ed.). Standard M07, 112
  • Drapkin, E. (1963). Effect of Rapana bezoar Linne (Mollusca, Muricidae) on the Black Sea fauna. Doklady Akademii Nauk SRR.
  • Fuentes, A., Fernández-Segovia, I., Escriche, I. & Serra, J. A. (2009). Comparison of physico-chemical parameters and composition of mussels (Mytilus galloprovincialis Lmk.) from different Spanish origins. Food Chemistry, 112(2): 295-302. https://doi.org/https://doi.org/ 10.1016/j.foodchem.2008.05.064
  • Gedik, K. (2018a). Bioaccessibility of Cd, Cr, Cu, Mn, Ni, Pb, and Zn in Mediterranean mussel (Mytilus galloprovincialis Lamarck, 1819) along the southeastern Black Sea coast. Human and Ecological Risk Assessment: An International Journal, 24(3): 754-766. https://doi.org/10.1080/10807039.2017.1398632
  • Gedik, K. (2018b). Bioaccessibility of heavy metals in rapa whelk Rapana venosa (Valenciennes, 1846): Assessing human health risk using an in vitro digestion model. Human and Ecological Risk Assessment: An International Journal, 24(1): 202-213. https://doi.org/10.1080/10807039.2017.1373329
  • Gul-Seker, M. & Mater, Y. (2009). Assessment of metal and antibiotic-resistance in marine bacteria isolated from Izmit Bay and Bosphorus entrance of Marmara and Black Sea, Turkey. Fresenius Environmental Bulletin, 18(11A): 2192-2202.
  • Kacar, A. (2011). Some microbial characteristics of mussels (Mytilus galloprovincialis) in coastal city area. Environmental Science and Pollution Research, 18(8): 1384. https://doi.org/10.1007/s11356-011-0487-3
  • Li, X., Gu, A. Z., Zhang, Y., Xie, B., Li, D. & Chen, J. (2019). Sub-lethal concentrations of heavy metals induce antibiotic resistance via mutagenesis. Journal of Hazardous Materials, 369: 9-16. https://doi.org/10.1016/j.jhazmat.2019.02.006
  • Matyar, F., Akkan, T., Uçak, Y. & Eraslan, B. (2010). Aeromonas and Pseudomonas: antibiotic and heavy metal resistance species from Iskenderun Bay, Turkey (northeast Mediterranean Sea). Environmental Monitoring and Assessment, 167(1-4): 309-320. https://doi.org/10.1007/s10661-009-1051-1
  • Matyar, F., Eraslan, B., Akkan, T., Kaya, A. & Dinçer, S. (2009). İskenderun Körfezi balıklarından izole edilen bakterilerde antibiyotik ve ağır metal dirençliliklerinin araştırılması. Biyoloji Bilimleri Araştırma Dergisi, 2(2), 1-5.
  • Misra, T. K., Brown, N. L., Fritzinger, D. C., Pridmore, R. D., Barnes, W. M., Haberstroh, L. & Silver, S. (1984). Mercuric ion-resistance operons of plasmid R100 and transposon Tn501: The beginning of the operon including the regulatory region and the first two structural genes. Proceedings of the National Academy of Sciences, 81(19): 5975-5979. https://doi.org/10.1073/ pnas.81.19.5975
  • Nies, A., Nies, D. H. & Silver, S. (1990). Nucleotide sequence and expression of a plasmid-encoded chromate resistance determinant from Alcaligenes eutrophus. Journal of Biological Chemistry, 265(10): 5648-5653. https://www.jbc.org/content/265/10/5648.long
  • Nies, D. H. (1999). Microbial heavy-metal resistance. Applied Microbiology and Biotechnology, 51(6): 730-750. https://doi.org/10.1007/s002530051457
  • Nieto, J., Ventosa, A. & Ruiz-Berraquero, F. (1987). Susceptibility of halobacteria to heavy metals. Applied Environmental and Public Health Microbiology, 53(5): 1199-1202.
  • Saglam, H., Kutlu, S., Dagtekin, M., Bascinar, S., Sahin, A., Selen, H. & Duzgunes, E. (2015). Population biology of Rapana venosa (Valenciennes, 1846) (Gastropoda: Neogastropoda) in the south-eastern Black Sea of Turkey. Cahiers de Biologie Marine, 56(4): 363-368. https://doi.org/10.21411/CBM.A.2A889E43
  • Sipahi, N., Mutlu, C. & Akkan, T. (2013). Antibiotic and heavy metal resistance levels of Enterobacteriaceae isolated from retail fishes in Giresun. Gıda, 38(6): 343-349. https://doi.org/10.5505/gida.2013.55264
  • Terzi, E. (2018a). Antimicrobial resistance profiles and tetracycline resistance genes of Escherichia coli in Mediterranean mussel and sea snails collected from Black Sea, Turkey. Alinteri Journal of Agriculture Sciences, 33(1): 43-49. https://doi.org/10.28955/alinterizbd.355019
  • Terzi, E. (2018b). Determination of antimicrobial resistance profiles of the bacteria isolated from cultured sturgeons. Menba Kastamonu University Faculty of Fisheries Journal, 4(2): 7-13.
  • Terzi, E. & Isler, H. (2019). Antibiotic resistance genes of Escherichia coli in coastal marine environment of Eastern Black Sea, Turkey. Fresenius Environmental Bulletin, 28(2A): 1594-1601.
  • Toroglu, S. & Dincer, S. (2009). Heavy metal resistances of Enterobacteriaceae from Aksu River (Turkey) polluted with different sources. Asian Journal of Chemistry, 21(1): 411-420.
  • Tsi, C., Ma, X., Lou, Z. & Zhang, F. (1983). Illustrations of the fauna of China (Mollusca). (2nd Ed.) Science Press, Beijing, China. 150p.
  • Ture, M., Kilic, M. B. & Altinok, I. (2020). Relationship between heavy metal accumulation in fish muscle and heavy metal resistance genes in bacteria isolated from fish. Biological Trace Element Research, https://doi.org/10.1007/s12011-020-02246-0
  • Yang, S., Deng, W., Liu, S., Yu, X., Mustafa, G. R., Chen, S., He, L., Ao, X., Yang, Y., Zhou, K., Li, B., Han, X., Xu, X. & Zou, L. (2020). Presence of heavy metal resistance genes in Escherichia coli and Salmonella, and analysis of resistance gene structure in E. coli E308. Journal of Global Antimicrobial Resistance, 21: 420-426. https://doi.org/https://doi.org/10.1016/j.jgar.2020.01.009
Yıl 2021, Cilt: 10 Sayı: 1, 36 - 41, 31.03.2021
https://doi.org/10.33714/masteb.776902

Öz

Proje Numarası

2015.53006.103.02.04

Kaynakça

  • Abou-Shanab, R. A. I., van Berkum, P. & Angle, J. S. (2007). Heavy metal resistance and genotypic analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale. Chemosphere, 68(2): 360-367. https://doi.org/10.1016/j.chemosphere.2006. 12.051
  • Abskharon, R. N. N., Hassan, S. H. A., Gad El-Rab, S. M. F. & Shoreit, A. A. M. (2008). Heavy metal resistant of E. coli isolated from wastewater sites in Assiut City, Egypt. Bulletin of Environmental Contamination and Toxicology, 81(3): 309. https://doi.org/10.1007/s00128-008-9494-6
  • Akçay, M. & Moon, C. J. (2004). The environmental impact of mining in the Pontides, Turkey: Reconnaissance sampling and GIS-based analysis. Geochemistry: Exploration, Environment, Analysis, 4(4): 317-328. https://doi.org/10.1144/1467-7873/03-052
  • Akinbowale, O. L., Peng, H., Grant, P. & Barton, M. D. (2007). Antibiotic and heavy metal resistance in motile aeromonads and pseudomonads from rainbow trout (Oncorhynchus mykiss) farms in Australia. International Journal of Antimicrobial Agents, 30(2): 177-182. https://doi.org/10.1016/j.ijantimicag.2007.03.012
  • Avşar, C. & Berber, İ. (2014). Plasmid profiling and antibiotics resistance of Escherichia coli strains isolated from Mytilus galloprovincialis and seawater. Journal of Coastal Life Medicine, 2(9): 689-693. https://doi.org/10.12980/JCLM.2.2014JCLM-2014-0069
  • Baltas, H., Sirin, M., Dalgic, G., Bayrak, E. Y. & Akdeniz, A. (2017). Assessment of metal concentrations (Cu, Zn, and Pb) in seawater, sediment and biota samples in the coastal area of Eastern Black Sea, Turkey. Marine Pollution Bulletin, 122(1-2): 475-482. https://doi.org/10.1016/j.marpolbul.2017.06.059
  • Bat, L. & Öztekin, H. C. (2016). Heavy metals in Mytilus galloprovincialis, Rapana venosa and Eriphia verrucosa from the Black Sea coasts of Turkey as bioindicators of pollution. Walailak Journal of Science and Technology, 13(9): 715-728.
  • Boran, H., Terzi, E., Altinok, I., Capkin, E. & Bascinar, N. (2013). Bacterial diseases of cultured Mediterranean horse mackerel (Trachurus mediterraneus) in sea cages. Aquaculture, 396: 8-13. https://doi.org/10.1016/ j.aquaculture.2013.02.025
  • Capkin, E., Ozdemir, S., Ozturk, R. C. & Altinok, I. (2017). Determination and transferability of plasmid‐mediated antibiotic resistance genes of the bacteria isolated from rainbow trout. Aquaculture Research, 48(11): 5561-5575.
  • Capkin, E., Terzi, E. & Altinok, I. (2015). Occurrence of antibiotic resistance genes in culturable bacteria isolated from Turkish trout farms and their local aquatic environment. Diseases of Aquatic Organisms, 114(2): 127-137. https://doi.org/10.3354/dao02852
  • Chapman, J. S. (2003). Disinfectant resistance mechanisms, cross-resistance, and co-resistance. International Biodeterioration & Biodegradation, 51(4): 271-276. https://doi.org/10.1016/S0964-8305(03)00044-1
  • CLSI (Clinical and Laboratory Standards Institute). (2018). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, (11th Ed.). Standard M07, 112
  • Drapkin, E. (1963). Effect of Rapana bezoar Linne (Mollusca, Muricidae) on the Black Sea fauna. Doklady Akademii Nauk SRR.
  • Fuentes, A., Fernández-Segovia, I., Escriche, I. & Serra, J. A. (2009). Comparison of physico-chemical parameters and composition of mussels (Mytilus galloprovincialis Lmk.) from different Spanish origins. Food Chemistry, 112(2): 295-302. https://doi.org/https://doi.org/ 10.1016/j.foodchem.2008.05.064
  • Gedik, K. (2018a). Bioaccessibility of Cd, Cr, Cu, Mn, Ni, Pb, and Zn in Mediterranean mussel (Mytilus galloprovincialis Lamarck, 1819) along the southeastern Black Sea coast. Human and Ecological Risk Assessment: An International Journal, 24(3): 754-766. https://doi.org/10.1080/10807039.2017.1398632
  • Gedik, K. (2018b). Bioaccessibility of heavy metals in rapa whelk Rapana venosa (Valenciennes, 1846): Assessing human health risk using an in vitro digestion model. Human and Ecological Risk Assessment: An International Journal, 24(1): 202-213. https://doi.org/10.1080/10807039.2017.1373329
  • Gul-Seker, M. & Mater, Y. (2009). Assessment of metal and antibiotic-resistance in marine bacteria isolated from Izmit Bay and Bosphorus entrance of Marmara and Black Sea, Turkey. Fresenius Environmental Bulletin, 18(11A): 2192-2202.
  • Kacar, A. (2011). Some microbial characteristics of mussels (Mytilus galloprovincialis) in coastal city area. Environmental Science and Pollution Research, 18(8): 1384. https://doi.org/10.1007/s11356-011-0487-3
  • Li, X., Gu, A. Z., Zhang, Y., Xie, B., Li, D. & Chen, J. (2019). Sub-lethal concentrations of heavy metals induce antibiotic resistance via mutagenesis. Journal of Hazardous Materials, 369: 9-16. https://doi.org/10.1016/j.jhazmat.2019.02.006
  • Matyar, F., Akkan, T., Uçak, Y. & Eraslan, B. (2010). Aeromonas and Pseudomonas: antibiotic and heavy metal resistance species from Iskenderun Bay, Turkey (northeast Mediterranean Sea). Environmental Monitoring and Assessment, 167(1-4): 309-320. https://doi.org/10.1007/s10661-009-1051-1
  • Matyar, F., Eraslan, B., Akkan, T., Kaya, A. & Dinçer, S. (2009). İskenderun Körfezi balıklarından izole edilen bakterilerde antibiyotik ve ağır metal dirençliliklerinin araştırılması. Biyoloji Bilimleri Araştırma Dergisi, 2(2), 1-5.
  • Misra, T. K., Brown, N. L., Fritzinger, D. C., Pridmore, R. D., Barnes, W. M., Haberstroh, L. & Silver, S. (1984). Mercuric ion-resistance operons of plasmid R100 and transposon Tn501: The beginning of the operon including the regulatory region and the first two structural genes. Proceedings of the National Academy of Sciences, 81(19): 5975-5979. https://doi.org/10.1073/ pnas.81.19.5975
  • Nies, A., Nies, D. H. & Silver, S. (1990). Nucleotide sequence and expression of a plasmid-encoded chromate resistance determinant from Alcaligenes eutrophus. Journal of Biological Chemistry, 265(10): 5648-5653. https://www.jbc.org/content/265/10/5648.long
  • Nies, D. H. (1999). Microbial heavy-metal resistance. Applied Microbiology and Biotechnology, 51(6): 730-750. https://doi.org/10.1007/s002530051457
  • Nieto, J., Ventosa, A. & Ruiz-Berraquero, F. (1987). Susceptibility of halobacteria to heavy metals. Applied Environmental and Public Health Microbiology, 53(5): 1199-1202.
  • Saglam, H., Kutlu, S., Dagtekin, M., Bascinar, S., Sahin, A., Selen, H. & Duzgunes, E. (2015). Population biology of Rapana venosa (Valenciennes, 1846) (Gastropoda: Neogastropoda) in the south-eastern Black Sea of Turkey. Cahiers de Biologie Marine, 56(4): 363-368. https://doi.org/10.21411/CBM.A.2A889E43
  • Sipahi, N., Mutlu, C. & Akkan, T. (2013). Antibiotic and heavy metal resistance levels of Enterobacteriaceae isolated from retail fishes in Giresun. Gıda, 38(6): 343-349. https://doi.org/10.5505/gida.2013.55264
  • Terzi, E. (2018a). Antimicrobial resistance profiles and tetracycline resistance genes of Escherichia coli in Mediterranean mussel and sea snails collected from Black Sea, Turkey. Alinteri Journal of Agriculture Sciences, 33(1): 43-49. https://doi.org/10.28955/alinterizbd.355019
  • Terzi, E. (2018b). Determination of antimicrobial resistance profiles of the bacteria isolated from cultured sturgeons. Menba Kastamonu University Faculty of Fisheries Journal, 4(2): 7-13.
  • Terzi, E. & Isler, H. (2019). Antibiotic resistance genes of Escherichia coli in coastal marine environment of Eastern Black Sea, Turkey. Fresenius Environmental Bulletin, 28(2A): 1594-1601.
  • Toroglu, S. & Dincer, S. (2009). Heavy metal resistances of Enterobacteriaceae from Aksu River (Turkey) polluted with different sources. Asian Journal of Chemistry, 21(1): 411-420.
  • Tsi, C., Ma, X., Lou, Z. & Zhang, F. (1983). Illustrations of the fauna of China (Mollusca). (2nd Ed.) Science Press, Beijing, China. 150p.
  • Ture, M., Kilic, M. B. & Altinok, I. (2020). Relationship between heavy metal accumulation in fish muscle and heavy metal resistance genes in bacteria isolated from fish. Biological Trace Element Research, https://doi.org/10.1007/s12011-020-02246-0
  • Yang, S., Deng, W., Liu, S., Yu, X., Mustafa, G. R., Chen, S., He, L., Ao, X., Yang, Y., Zhou, K., Li, B., Han, X., Xu, X. & Zou, L. (2020). Presence of heavy metal resistance genes in Escherichia coli and Salmonella, and analysis of resistance gene structure in E. coli E308. Journal of Global Antimicrobial Resistance, 21: 420-426. https://doi.org/https://doi.org/10.1016/j.jgar.2020.01.009
Toplam 34 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Hidrobiyoloji
Bölüm Makaleler
Yazarlar

Ertuğrul Terzi 0000-0003-2811-6497

Fatih Civelek 0000-0002-8881-8098

Proje Numarası 2015.53006.103.02.04
Yayımlanma Tarihi 31 Mart 2021
Gönderilme Tarihi 4 Ağustos 2020
Kabul Tarihi 1 Ekim 2020
Yayımlandığı Sayı Yıl 2021 Cilt: 10 Sayı: 1

Kaynak Göster

APA Terzi, E., & Civelek, F. (2021). Cu, Cd, As and Hg resistance levels in Escherichia coli isolated from Mediterranean mussel and sea snail in the Southeastern Black Sea. Marine Science and Technology Bulletin, 10(1), 36-41. https://doi.org/10.33714/masteb.776902
AMA Terzi E, Civelek F. Cu, Cd, As and Hg resistance levels in Escherichia coli isolated from Mediterranean mussel and sea snail in the Southeastern Black Sea. Mar. Sci. Tech. Bull. Mart 2021;10(1):36-41. doi:10.33714/masteb.776902
Chicago Terzi, Ertuğrul, ve Fatih Civelek. “Cu, Cd, As and Hg Resistance Levels in Escherichia Coli Isolated from Mediterranean Mussel and Sea Snail in the Southeastern Black Sea”. Marine Science and Technology Bulletin 10, sy. 1 (Mart 2021): 36-41. https://doi.org/10.33714/masteb.776902.
EndNote Terzi E, Civelek F (01 Mart 2021) Cu, Cd, As and Hg resistance levels in Escherichia coli isolated from Mediterranean mussel and sea snail in the Southeastern Black Sea. Marine Science and Technology Bulletin 10 1 36–41.
IEEE E. Terzi ve F. Civelek, “Cu, Cd, As and Hg resistance levels in Escherichia coli isolated from Mediterranean mussel and sea snail in the Southeastern Black Sea”, Mar. Sci. Tech. Bull., c. 10, sy. 1, ss. 36–41, 2021, doi: 10.33714/masteb.776902.
ISNAD Terzi, Ertuğrul - Civelek, Fatih. “Cu, Cd, As and Hg Resistance Levels in Escherichia Coli Isolated from Mediterranean Mussel and Sea Snail in the Southeastern Black Sea”. Marine Science and Technology Bulletin 10/1 (Mart 2021), 36-41. https://doi.org/10.33714/masteb.776902.
JAMA Terzi E, Civelek F. Cu, Cd, As and Hg resistance levels in Escherichia coli isolated from Mediterranean mussel and sea snail in the Southeastern Black Sea. Mar. Sci. Tech. Bull. 2021;10:36–41.
MLA Terzi, Ertuğrul ve Fatih Civelek. “Cu, Cd, As and Hg Resistance Levels in Escherichia Coli Isolated from Mediterranean Mussel and Sea Snail in the Southeastern Black Sea”. Marine Science and Technology Bulletin, c. 10, sy. 1, 2021, ss. 36-41, doi:10.33714/masteb.776902.
Vancouver Terzi E, Civelek F. Cu, Cd, As and Hg resistance levels in Escherichia coli isolated from Mediterranean mussel and sea snail in the Southeastern Black Sea. Mar. Sci. Tech. Bull. 2021;10(1):36-41.

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