Skip to content
1887
Volume 64, Issue 4
  • ISSN: 2056-5135

Abstract

Heavy metal and antibiotic-resistant bacteria have potential for environmental bioremediation applications. Resistant bacteria were investigated in sediment and seawater samples taken from the Aegean Sea, Turkey, between 2011 and 2013. Bioindicator bacteria in seawater samples were tested using the membrane filtration technique. The spread plate technique and VITEK® 2 Compact 30 micro identification system were used for heterotrophic aerobic bacteria in the samples. The minimum inhibition concentration method was used for heavy metal-resistant bacteria. Antibiotic-resistant bacteria were tested using the disk diffusion method. All bacteria isolated from sediment samples showed 100% resistance to rifampicin, sulfonamide, tetracycline and ampicillin. 98% of isolates were resistant against nitrofurantoin and oxytetracycline. Higher antibiotic and heavy metal resistance was recorded in bacteria isolated from sediment than seawater samples. The highest levels of bacterial metal resistance were recorded against copper (58.3%), zinc (33.8%), lead (32.1%), chromium (31%) and iron (25.2%). The results show that antibiotic and heavy metal resistance in bacteria from sediment and seawater can be observed as responses to environmental influences including pollution in marine areas.

Loading

Article metrics loading...

/content/journals/10.1595/205651320X15953337767424
2020-01-01
2024-12-09
Loading full text...

Full text loading...

/deliver/fulltext/jmtr/64/4/Altug_16a_Imp.html?itemId=/content/journals/10.1595/205651320X15953337767424&mimeType=html&fmt=ahah

References

  1. D. A. Rouch, B. T. O. Lee, A. P. Morby, J. Ind. Microbiol., 1995, 14, (2), 132 LINK https://doi.org/10.1007/bf01569895 [Google Scholar]
  2. S. Congeevaram, S. Dhanarani, J. Park, M. Dexilin, K. Thamaraiselvi, J. Hazard. Mater., 2007, 146, (1–2), 270 LINK https://doi.org/10.1016/j.jhazmat.2006.12.017 [Google Scholar]
  3. M. R. Bruins, S. Kapil, F. W. Oehme, Ecotoxicol. Environ. Saf., 2000, 45, (3), 198 LINK https://doi.org/10.1006/eesa.1999.1860 [Google Scholar]
  4. E. E. Bestawy, S. Helmy, H. Hussien, M. Fahmy, R. Amer, Appl. Water Sci., 2012, 3, (1), 181 LINK https://doi.org/10.1007/s13201-012-0071-0 [Google Scholar]
  5. H. K. Allen, J. Donato, H. H. Wang, K. A. Cloud-Hansen, J. Davies, J. Handelsman, Nat. Rev. Microbiol., 2010, 8, (4), 251 LINK https://doi.org/10.1038/nrmicro2312 [Google Scholar]
  6. H. H. Wang, D. W. Schaffner, Appl. Environ. Microbiol., 2011, 77, (20), 7093 LINK https://doi.org/10.1128/AEM.06565-11 [Google Scholar]
  7. N. Rosenblatt-Farrell, Environ. Health Perspect., 2009, 117, (6), A244 LINK https://doi.org/10.1289/ehp.117-a244 [Google Scholar]
  8. K. Kümmerer, J. Antimicrob. Chemother., 2004, 54, (2), 311 LINK https://doi.org/10.1093/jac/dkh325 [Google Scholar]
  9. S. Kim, D. S. Aga, J. Toxicol. Environ. Health: Part B, 2007, 10, (8), 559 LINK https://doi.org/10.1080/15287390600975137 [Google Scholar]
  10. A. J. Watkinson, G. B. Micalizzi, G. M. Graham, J. B. Bates, S. D. Costanzo, Appl. Environ. Microbiol., 2007, 73, (17), 5667 LINK https://doi.org/10.1128/AEM.00763-07 [Google Scholar]
  11. J. L. Caplin, G. W. Hanlon, H. D. Taylor, Environ. Microbiol., 2008, 10, (4), 885 LINK https://doi.org/10.1111/j.1462-2920.2007.01507.x [Google Scholar]
  12. L. Nonaka, K. Ikeno, S. Suzuki, Microbes Environ., 2007, 22, (4), 355 LINK https://doi.org/10.1264/jsme2.22.355 [Google Scholar]
  13. P. T. P. Hoa, L. Nonaka, P. Hung Viet, S. Suzuki, Sci. Total Environ., 2008, 405, (1–3), 377 LINK https://doi.org/10.1016/j.scitotenv.2008.06.023 [Google Scholar]
  14. D. I. Andersson, D. Hughes, Nat. Rev. Microbiol., 2010, 8, (4), 260 LINK https://doi.org/10.1038/nrmicro2319 [Google Scholar]
  15. S. Squadrone, Environ. Monit. Assess., 2020, 192, (4), 238 LINK https://doi.org/10.1007/s10661-020-8191-8 [Google Scholar]
  16. M. L. Nadimpalli, S. J. Marks, M. C. Montealegre, R. H. Gilman, M. J. Pajuelo, M. Saito, P. Tsukayama, S. M. Njenga, J. Kiiru, J. Swarthout, M. A. Islam, T. R. Julian, A. J. Pickering, Nat. Microbiol., 2020, 5, (6), 787 LINK https://doi.org/10.1038/s41564-020-0722-0 [Google Scholar]
  17. G. Altug, N. Balkis, Environ. Monit. Assess., 2009, 149, (1–4), 61 LINK https://doi.org/10.1007/s10661-008-0183-z [Google Scholar]
  18. M. Imran, K. R. Das, M. M. Naik, Chemosphere, 2019, 215, 846 LINK https://doi.org/10.1016/j.chemosphere.2018.10.114 [Google Scholar]
  19. P. Laganà, G. Caruso, I. Corsi, E. Bergami, V. Venuti, D. Majolino, R. La Ferla, M. Azzaro, S. Cappello, Int. J. Hyg. Environ. Health, 2019, 222, (1), 89 LINK https://doi.org/10.1016/j.ijheh.2018.08.009 [Google Scholar]
  20. G. Lunde, Environ. Health Perspect., 1977, 19, 47 LINK https://doi.org/10.1289/ehp.771947 [Google Scholar]
  21. A. Hernández, R. P. Mellado, J. L. Martínez, Appl. Environ. Microbiol., 1998, 64, (11), 4317 LINK https://doi.org/10.1128/aem.64.11.4317-4320.1998 [Google Scholar]
  22. L. D. Rasmussen, S. J. Sørensen, Curr. Microbiol., 1998, 36, (5), 291 LINK https://doi.org/10.1007/s002849900312 [Google Scholar]
  23. D. H. Nies, Appl. Microbiol. Biotechnol., 1999, 51, (6), 730 LINK https://doi.org/10.1007/s002530051457 [Google Scholar]
  24. G. Altuğ, M. Çardak, P. S. Ciftci, J. Fish. Aquat. Sci., 2007, 22, (23), 39 (in Turkish) [Google Scholar]
  25. G. Altuğ, M. Çardak, P. S. Ciftci, S. Gürün, S. Kalkan, ‘Bacterial Diversity in Güllük Bay’, Tübitak Project Workshop, 10th May, 2013, Güllük, Muğla, Turkey, ed. G. Altuğ, Istanbul University, Turkey, 2013, pp. 3–7 (in Turkish) [Google Scholar]
  26. S. Kalkan, G. Altuğ, Mar. Pollut. Bull., 2015, 95, (1), 380 LINK https://doi.org/10.1016/j.marpolbul.2015.04.017 [Google Scholar]
  27. H. Yıldız, H. M. Doğan, Ö. Urla, Tarla Bit. Merk. Arş. Ens. Derg., 2002, 11, (1–2), 142 (in Turkish) LINK https://dergipark.org.tr/en/pub/tarbitderg/issue/11510/137077 [Google Scholar]
  28. A. Demirak, A. Balci, Ö. Dalman, M. Tüfekçi, Water Air Soil Pollut., 2005, 162, (1–4), 171 LINK https://doi.org/10.1007/s11270-005-5999-3 [Google Scholar]
  29. A. Baba, A. Kaya, Y. K. Birsoy, Water Air Soil Pollut., 2003, 149, (1–4), 93 LINK https://doi.org/10.1023/a:1025660629875 [Google Scholar]
  30. P. Çiftçi, G. Altuğ, M. Çardak, S. Gürün, ‘Distribution of Indicator Bacteria in Recreational and Fish Farming Areas of Gulluk Bay, Turkey’, Effective Utilization of Ocean Resources and Future Maritime Industries, Tokyo, Japan, 2nd–11th November, 2011, Tokyo University of Marine Science and Technology (TUMSAT), Japan, p. 25 [Google Scholar]
  31. A. Demirak, A. Balci, M. Tüfekçi, Environ. Monit. Assess., 2006, 123, (1–3), 1 LINK http://dx.doi.org/10.1007/s10661-005-9063-y [Google Scholar]
  32. İ. Atılgan, Ö. Egemen, Ege J. Fish. Aquat. Sci., 2001, 18, (1–2), 225 LINK http://www.egejfas.org/en/pub/issue/5025/68374 [Google Scholar]
  33. G. Yucel-Gier, I. Pazi, F. Kucuksezgin, Turk. J. Fish. Aquat. Sci., 2013, 13, (4), 737 LINK http://www.trjfas.org/abstract.php?id=188 [Google Scholar]
  34. E. Marti, E. Variatza, J. L. Balcazar, Trends Microbiol., 2014, 22, (1), 36 LINK https://doi.org/10.1016/j.tim.2013.11.001 [Google Scholar]
  35. K. P. Acharya, R. T. Wilson, Front. Med., 2019, 6, 105 LINK https://doi.org/10.3389/fmed.2019.00105 [Google Scholar]
  36. S. A. Kraemer, A. Ramachandran, G. G. Perron, Microorganisms, 2019, 7, (6), 180 LINK https://doi.org/10.3390/microorganisms7060180 [Google Scholar]
  37. A. Olgun, ‘Evaluation in Terms of Vessels and Ballast Waters entering Güllük Bay’, Bacteriology of Güllük Bay, Tübitak Project Workshop, 10th May, 2013, Güllük, Muğla, Turkey, ed. G. Altuğ, Istanbul University, Turkey, pp. 33–37 (in Turkish) [Google Scholar]
  38. “Standard Methods for the Examination of Water and Waste Water”, eds. E. W. Rice, R. B. Baird, A. D. Eaton, L. S. Clesceri, 22nd Edn., American Public Health Association, American Water Works Association, Water Environment Federation, 2012 [Google Scholar]
  39. D. H. Pincus, ‘Microbial Identification Using the bioMérıeux VITEK® 2 System’, in “Encyclopedia of Rapid Microbiological Methods”, ed. M. J. Miller, Vol. 2, Parenteral Drug Association, Bethesda, USA, 2006, pp. 1–32 [Google Scholar]
  40. P. A. Sobecky, T. J. Mincer, M. C. Chang, A. Toukdarian, D. R. Helinski, Appl. Environ. Microbiol., 1998, 64, (8), 2822 LINK https://doi.org/10.1128/aem.64.8.2822-2830.1998 [Google Scholar]
  41. M. A. Wikler, F. R. Cockerill, W. A. Craig, M. N. Dudley, G. M. Eliopoulos, D. W. Hecht, J. F. Hindler, D. E. Low, D. J. Sheehan, F. C. Tenover, J. D. Turnidge, M. P. Weinstein, B. L. Zimmer, M. J. Ferraro, J. M. Swenson, ‘Performance Standards for Antimicrobial Susceptibility Testing: Sixteenth Informational Supplement’, M100– S16, Clinical and Laboratory Standards Institute, Wayne, USA, 2006, 192 pp [Google Scholar]
  42. P. H. Krumperman, Appl. Environ. Microbiol., 1983, 46, (1), 165 LINK https://doi.org/10.1128/aem.46.1.165-170.1983 [Google Scholar]
  43. J. A. Washington, V. L. Sutter, ‘Dilution Test Procedures’, in “Manual of Clinical Microbiology”, eds. E. H. Lennette, A. Balows, W. J. Hausler, J. P. Truant, American Society for Microbiology, Washington, DC, USA, 1981, pp 549–555 [Google Scholar]
  44. A. D. Geiselbrecht, R. P. Herwig, J. W. Deming, J. T. Staley, Appl. Environ. Microbiol., 1996, 62, (9), 3344 LINK https://doi.org/10.1128/aem.62.9.3344-3349.1996 [Google Scholar]
  45. V. Perreten, P. Boerlin, Antimicrob. Agents Chemother., 2003, 47, (3), 1169 LINK https://doi.org/10.1128/aac.47.3.1169-1172.2003 [Google Scholar]
  46. T. X. Le, Y. Munekage, S. Kato, Sci. Total Environ., 2005, 349, (1–3), 95 LINK https://doi.org/10.1016/j.scitotenv.2005.01.006 [Google Scholar]
  47. M. T. Blahna, C. A. Zalewski, J. Reuer, G. Kahlmeter, B. Foxman, C. F. Marrs, J. Antimicrob. Chemother., 2006, 57, (4), 666 LINK https://doi.org/10.1093/jac/dkl020 [Google Scholar]
  48. Y. Agersø, A. Petersen, J. Antimicrob. Chemother., 2007, 59, (1), 23 LINK https://doi.org/10.1093/jac/dkl419 [Google Scholar]
  49. A. H. Buschmann, A. Tomova, A. López, M. A. Maldonado, L. A. Henríquez, L. Ivanova, F. Moy, H. P. Godfrey, F. C. Cabello, PLoS One, 2012, 7, (8), e42724 LINK https://doi.org/10.1371/journal.pone.0042724 [Google Scholar]
  50. J. Kerry, R. Coyne, D. Gilroy, M. Hiney, P. Smith, Aquaculture, 1996, 145, (1–4), 31 LINK https://doi.org/10.1016/s0044-8486(96)01353-1 [Google Scholar]
  51. F. Matyar, A. Kaya, S. Dinçer, Sci. Total Environ., 2008, 407, (1), 279 LINK https://doi.org/10.1016/j.scitotenv.2008.08.014 [Google Scholar]
  52. Z. J. Mudryk, Mar. Pollut. Bull., 2005, 50, (1), 80 LINK https://doi.org/10.1016/j.marpolbul.2004.10.001 [Google Scholar]
  53. H. Sørum, Acta Vet. Scand. Suppl., 1999, 92, 29 [Google Scholar]
  54. V. Inglis, ‘Antibacterial Chemotherapy in Aquaculture: Review of Practice, Associated Risks and Need for Action’, Use of Chemicals in Aquaculture in Asia, Tigbauan, Philippines, 20th–22nd May, 1996, “Proceedings of the Meeting on the Use of Chemicals in Aquaculture in Asia”, eds. J. R. Arthur, C. R. Larilla-Pitogo, R. P. Subasinghe, Southeast Asian Fisheries Development Center Aquaculture Department, Tigbauan, Philippines, 2000, pp. 7–22 LINK http://hdl.handle.net/10862/611 [Google Scholar]
  55. G. Rhodes, G. Huys, J. Swings, P. McGann, M. Hiney, P. Smith, R. W. Pickup, Appl. Environ. Microbiol., 2000, 66, (9), 3883 LINK https://doi.org/10.1128/aem.66.9.3883-3890.2000 [Google Scholar]
  56. Y. Huang, L. Zhang, L. Tiu, H. H. Wang, Front. Microbiol., 2015, 6, 914 LINK https://doi.org/10.3389/fmicb.2015.00914 [Google Scholar]
  57. P.-R. Hsueh, L.-J. Teng, P.-C. Yang, Y.-C. Chen, H.-J. Pan, S.-W. Ho, K.-T. Luh, Clin. Infect. Dis., 1998, 26, (3), 676 LINK https://doi.org/10.1086/514595 [Google Scholar]
  58. C. Baker-Austin, M. S. Wright, R. Stepanauskas, J. V. McArthur, Trends Microbiol., 2006, 14, (4), 176 LINK https://doi.org/10.1016/j.tim.2006.02.006 [Google Scholar]
  59. P. R. Jensen, W. Fenical, Annu. Rev. Microbiol., 1994, 48, 559 LINK https://doi.org/10.1146/annurev.mi.48.100194.003015 [Google Scholar]
  60. D. Claus, R. C. W. Berkeley, ‘Genus Bacillus, Cohn 1872’, in “Bergey’s Manual of Systematic Bacteriology” eds. P. H. A. Sneath , N. S. Mair, M. E. Sharpe, J. G. Holt, Vol. 2, Williams and Wilkins Co, Baltimore, USA, 1986, pp 1105–1139 [Google Scholar]
  61. S. B. Levy, B. Marshall, Nat. Med., 2004, 10, (12), S122 LINK https://doi.org/10.1038/nm1145 [Google Scholar]
  62. D. G. Capone, D. P. Weston, V. Miller, C. Shoemaker, Aquaculture, 1996, 145, (1–4), 55 LINK https://doi.org/10.1016/s0044-8486(96)01330-0 [Google Scholar]
  63. F. M. Aarestrup, Basic Clin. Pharmacol. Toxicol., 2005, 96, (4), 271 LINK https://doi.org/10.1111/j.1742-7843.2005.pto960401.x [Google Scholar]
  64. N. van de Sande-Bruinsma, H. Grundmann, D. Verloo, E. Tiemersma, J. Monen, H. Goossens, M. Ferech, Emerg. Infect. Dis., 2008, 14, (11), 1722 LINK https://doi.org/10.3201/eid1411.070467 [Google Scholar]
  65. E. Gullberg, S. Cao, O. G. Berg, C. Ilbäck, L. Sandegren, D. Hughes, D. I. Andersson, PLoS Pathog., 2011, 7, (7), e1002158 LINK https://doi.org/10.1371/journal.ppat.1002158 [Google Scholar]
  66. C. P. Randall, A. Gupta, N. Jackson, D. Busse, A. J. O’Neill, J. Antimicrob. Chemother., 2015, 70, (4), 1037 LINK https://doi.org/10.1093/jac/dku523 [Google Scholar]
  67. L. A. M. Carneiro, A. P. S. Silva, V. L. C. Merquior, M. L. P. Queiroz, FEMS Microbiol. Lett., 2003, 228, (2), 175 LINK https://doi.org/10.1016/s0378-1097(03)00739-0 [Google Scholar]
  68. L. P. Randall, S. W. Cooles, M. K. Osborn, L. J. V. Piddock, M. J. Woodward, J. Antimicrob. Chemother., 2004, 53, (2), 208 LINK https://doi.org/10.1093/jac/dkh070 [Google Scholar]
  69. A. S. Schmidt, M. S. Bruun, I. Dalsgaard, J. L. Larsen, Appl. Environ. Microbiol., 2001, 67, (12), 5675 LINK https://doi.org/10.1128/AEM.67.12.5675-5682.2001 [Google Scholar]
  70. M. Teuber, Curr. Opin. Microbiol., 2001, 4, (5), 493 LINK https://doi.org/10.1016/s1369-5274(00)00241-1 [Google Scholar]
  71. S. Silver, L. T. Phung, Annu. Rev. Microbiol., 1996, 50, 753 LINK https://doi.org/10.1146/annurev.micro.50.1.753 [Google Scholar]
  72. F. Matyar, T. Akkan, Y. Uçak, B. Eraslan, Environ. Monit. Assess., 2010, 167, (1–4), 309 LINK https://doi.org/10.1007/s10661-009-1051-1 [Google Scholar]
  73. S. Silver, M. Walderhaug, Microbiol. Rev., 1992, 56, (1), 195 LINK https://doi.org/10.1128/mmbr.56.1.195-228.1992 [Google Scholar]
  74. H. Aiking, A. Stijnman, C. van Garderen, H. van Heerikhuizen, J. van ’t Riet, Appl. Environ. Microbiol., 1984, 47, (2), 374 LINK https://doi.org/10.1128/aem.47.2.374-377.1984 [Google Scholar]
  75. N. Çağlar, A. Aksu, G. Altuğ, Geol. Bull. Turkey, 2020, 63, (1), 117 LINK https://doi.org/10.25288/tjb.585304 [Google Scholar]
/content/journals/10.1595/205651320X15953337767424
Loading
/content/journals/10.1595/205651320X15953337767424
Loading

Data & Media loading...

  • Article Type: Research Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error
Please enter a valid_number test