Skip to main content
Log in

Isolation and Identification of Enterococci from Seawater Samples: Assessment of Their Resistance to Antibiotics and Heavy Metals

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

A hundred Enterococcus strains were isolated from seawater samples collected from coastal areas of Istanbul. Isolates were identified to the species level using standard biochemical tests specified by Facklam and Collins. The species distribution was as follows Enterococcus faecalis (96%), Enterococcus gallinarum (3%) and Enterococcus solitarius (1%). The resistance of bacteria to both heavy metals (zinc [Zn], iron [Fe], cadmium [Cd], chrome [Cr], cobalt [Co]) and antibiotics (ampicillin 10 μg [AP], penicillin G 10 Units [PG], gentamycin 10 μg [GM], streptomycin 10 μg [S], chloramphenicol 10 μg [C], erythromycin 15 μg [E], kanamycin 30 μg [K], amikacin 30 μg [AK], nalidixic acid 30 μg [NA], and vancomycin 30 μg [VA]) was evaluated. None of the strains was resistant to VA. It was found that among the 100 isolates, those that exhibit resistance to antibiotics, particularly NA, S and K, were also resistant all the heavy metals tested. To our knowledge this is the first report focusing on determination of resistance of environmental enterococci found in Istanbul against heavy metals and antibiotics. Thus, combined expressions of antibiotic and heavy metal resistance may help to reinforce ecological and epidemiological studies and to determine the role of these strains in antibiotic and heavy metal resistance dissemination.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Akgul, S. N., & Sumerkan, B. (1999). Identification of enterococci isolated from various clinical specimens based on biochemical characteristics. Turkish Journal of Infection, 13(3), 399–402.

    Google Scholar 

  • Aviles, M., De Vicente, A., Codina, J. C., & Romero, P. (1988). Antibiotic resistance of bacterial strains isolated from the marine environment. Rapport Commission Internationale Pour L’Exploration Scientifique De La Mer Méditerranée, 31, 173–174.

    Google Scholar 

  • Barisic, Z., & Punda-Polić, V. (2000). Antibiotic resistance among enterococcal strains isolated from clinical specimens. International Journal of Antimicrobial Agents, 16, 65–68.

    Article  CAS  Google Scholar 

  • Barry, A. L., & Thornsberry, C. (1981). Susceptibility testing. In E. H. Lennette, A. Balows, W. J. Hausler, & J. P. Truant (Eds.), Manual of clinical microbiology (pp. 561–574). Washington, District of Columbia: American Society for Microbiology.

    Google Scholar 

  • Bervoets, L., Int Panis, L., & Verheyen, R. (1994). Trace metal levels in water, sediments and Chironomus gr. thumni, from different water courses in Flanders (Belgium). Chemosphere, 29, 1591–1601.

    Article  CAS  Google Scholar 

  • Borrego, J. J., & José Figueras M. (1997). Microbiological quality of natural waters. Microbiología SEM, 13, 413–416.

    CAS  Google Scholar 

  • Cabelli, V. J., Dufour, P. A., Levin, M. A., Mc Cabe L. J., & Haberman, P. W. (1979). Relationship of microbial indicators to health effects at marine bathing beaches. American Journal of Public Health, 69(7), 690–696.

    CAS  Google Scholar 

  • Calomiris, J. J., Armstrong, J. L., & Seidler, R. J. (1984). Association of metal tolerance with multiple antibiotic resistance of bacteria isolated from drinking water. Applied and Environmental Microbiology, 47, 1238–1242.

    CAS  Google Scholar 

  • Chandrasekaran, S., Venkatesh, B., & Lalithakumari, D. (1998). Transfer and expression of a multiple antibiotic resistance plasmid in marine bacteria. Current Microbiology, 37, 347–351.

    Article  CAS  Google Scholar 

  • Choi, S., Chu, W., Brown, J., Becker, S. J., Harwood, V. J., & Jiang, S. C. (2003). Application of enterococci antibiotic resistance patterns for contamination source identification at Huntington Beach, California. Marine Pollution Bulletin, 46, 748–755.

    Article  CAS  Google Scholar 

  • De Vicente, A., Avilés, M., Codina, J. C., Borrego J. J., & Romero, P. (1990). Resistance to antibiotics and heavy metals of Pseudomonas aeruginosa isolated from natural waters. Journal of Applied Bacteriology, 68, 625–632.

    Google Scholar 

  • Dicuonzo, G., Gherardi, G., Lorino, G., Angeletti, S., Battistoni, F., Bertuccini, L., et al. (2001). Antibiotic resistance and genotypic characterization by PFGE of clinical and environmental isolates of enterococci. FEMS Microbiology Letters, 201, 205–211.

    Article  CAS  Google Scholar 

  • Dionisio, L. P. C., & Borrego, J. J. (1995). Evaluation of media for the enumeration of faecal streptococci from natural water samples. Journal of Microbiological Methods, 23(2), 183–203.

    Article  Google Scholar 

  • Eskiturk, A., Ekti, M., Culha, G., & Korten, V. (1997). Investigation of the prevalence of high level aminoglycoside resistant and vancomycin resistant enterococci among hospitalized patients and sewage samples. Bulletin of Microbiology, 31, 219–229.

    Google Scholar 

  • Facklam, R. R., & Collins, M. D. (1989). Identification of Enterococcus species isolated form human infections by a conventional test scheme. Journal of Clinical Microbiology, 27, 731–734.

    CAS  Google Scholar 

  • Fleisher, J. M., Kay, D., Jones, F., Wyer, M. D., & Godfree, A. F. (1996). Marine waters contaminated with domestic sewage: Nonenteric illnesses associated with bather exposure in the United Kingdom. American Journal of Public Health, 86(9), 1228–1234.

    Article  CAS  Google Scholar 

  • Genthner, F. J., James, J. B., Yates, D. F., & Friedman S. D. (2005). Use of composite data sets for source-tracking enterococci in the water column and shoreline interstitial waters on Pensacola Beach, Florida. Marine Pollution Bulletin, 50, 724–732.

    Article  CAS  Google Scholar 

  • Grewal, J. S., & Tiwari, R. P. (1990). Resistance to metal ions and antibiotics in Escherichia coli isolated from foodstuffs. Journal of Medical Microbiology, 32, 223–236.

    CAS  Google Scholar 

  • Haraguchi, H., & Akagi, T. (1991). Application of atomic absorption to marine analysis. In S. E. Manahan (Ed.), Environmental Chemistry (pp. 154–157). Michigan, America.

  • Hartke, A., Lemarinier, S., Pichereau, V., & Auffray, Y. (2002). Survival of Enterococcus faecalis in seawater microcosm is limited in the presence of bacteriovorous zooflagellates. Current Microbiology, 44, 329–335.

    Article  CAS  Google Scholar 

  • Holt, J. G., Krieg, N. R., Sneath, P. H. A., Staley, J. T., Williams, S. T. (1994). In W. R. Hensly (Ed.), Bergey’s manual of determinative bacteriology (9th edn.) (pp. 538–539). Baltimore, Maryland: Williams & Wilkins.

    Google Scholar 

  • Jana, S., & Bhattacharya, D. N. (1987). Effect of heavy metals on growth population of a fecal coliform bacterium Escherichia coli in aquatic environment. Water, Air, and Soil Pollution, 38, 251–254.

    Google Scholar 

  • Junco, M. T. T., Martín, M. G., Toledo, M. L. P., Gómez, P. L., & Barrasa, J. L. M. (2001). Identification and antibiotic resistance of faecal enterococci isolated from water samples. International Journal of Hygiene and Environmental Health, 203, 363–368.

    Article  CAS  Google Scholar 

  • Kacmaz, B., & Aksoy, A. (2005). Antimicrobial resistance of enterococci in Turkey. International Journal of Antimicrobial Agents, 25, 535–538.

    Article  CAS  Google Scholar 

  • Kim, J., Lee, G., Kim, Y., Kim, S., & Kim, Y. H. (2004). In vitro antibacterial activity of echinomycin and a novel analogue, YK2000, against vancomycin-resistant enterococci. International Journal of Antimicrobial Agents, 24, 613–615.

    Article  CAS  Google Scholar 

  • Kimiran, A. (2002). Assessment of the bacteriological quality of the coastal waters of Istanbul. University of Istanbul Faculty of Science the Journal of Biology, 65, 61–76.

    Google Scholar 

  • Klare, I., Konstabel, C., Badstübner, D., Werner, G., & Witte, W. (2003). Occurrence and spread of antibiotic resistances in Enterococcus faecium. International Journal of Food Microbiology, 88, 269–290.

    Article  CAS  Google Scholar 

  • Kühn, I., Iversen, A., Burman, L. G., Olsson-Liljequist, B., Franklin, A., Finn, M., et al. (2000). Epidemiology and ecology of enterococci, with special reference to antibiotic resistant strains, in animals, humans and the environment example of an ongoing project within the European Research Programme. International Journal of Antimicrobial Agents, 14, 337–342.

    Article  Google Scholar 

  • Laplace, J. M., Hartke, A., Giard, J. C., & Auffray, Y. (2000). Cloning, characterization and expression of an Enterococcus faecalis gene responsive to heavy metals. Applied Microbiology and Biotechnology, 53, 685–689.

    Article  CAS  Google Scholar 

  • Lleò M. M., Bonato, B., Benedetti, D., & Canepari, P. (2005). Survival of enterococcal species in aquatic environments. FEMS Microbiology, Ecology, 54(2), 189–196.

    Article  CAS  Google Scholar 

  • Lopes, M. F. S., Riberio, T., Abrantes, M., Marques J. J. F., Tenreiro, R., & Crespo, M. T. B. (2005). Antimicrobial resistance profiles of dairy and clinical isolates and type strains of enterococci. International Journal of Food Microbiology, 103, 191–198.

    Article  CAS  Google Scholar 

  • Manero, A., & Blanch, A. R. (1999). Identification of Enterococcus spp. with a biochemical key. Applied and Environmental Microbiology, 65(10), 4425–4430.

    CAS  Google Scholar 

  • Moaddab, S. B., & Toreci, K. (2000). Species level identification and investigation of resistance to vancomycin and some other antibiotics in Enterococcus strains. Journal of the Turkish Microbiological Society, 30, 77–84.

    Google Scholar 

  • Moreno, A., Diaz, J., Luzon, P., & Batista, N. (1997). Evaluation of a rapid method for the identification of the Enterococcus genus. Enfermedades Infecciosas y Microbiologia Clinica, 15(2), 85–87.

    CAS  Google Scholar 

  • Morozzi, G., Cenci, G., Caldini, G., Losito, G., & Morosi, A. (1986). Relationship between environment spread and presence in hosts of Escherichia coli strains resistant to antibiotics and metals. Zentralblatt fur Bakteriologie, Mikrobiologie und Hygiene. Serie B, 182, 393–400.

    CAS  Google Scholar 

  • Nakahara, H., Ishikawa, T., Sarai, Y., & Kondo, I. (1977). Distribution of resistance to metals and antibiotics of staphylococcal strains in Japan. Zentralblatt fur Bakteriologie, Mikrobiologie und Hygiene, 237, 470–476.

    CAS  Google Scholar 

  • National Committee for Clinical Laboratory Standards (2001). Performance standards for antimicrobial susceptibility testing. Eleventh International Supplement. Disk diffusion. M100-S 11. NCCLS, Villanova, Pennsylvania, USA.

  • Peters, J., Mac, Kiem, Wichmann-Schauer, H., Klein, G., & Ellerbroek, L. (2003). Species distribution and antibiotic resistance patterns of enterococci isolated from food of animal origin in Germany. International Journal of Food Microbiology, 88, 311–314.

    Article  CAS  Google Scholar 

  • Pourcher, A. M., Devriese, L. A., Hernandez, J. P., & Delattre, J. M. (1991). Enumeration by a miniaturized method of Escherichia coli, Streptococcus bovis and enterococci as indicators of the origin of fecal pollution of waters. Journal of Applied Bacteriology, 70, 525–530.

    CAS  Google Scholar 

  • Rosdahl, V. T., & Rosendal, K. (1980). Resistance to cadmium, arsenate and mercury among Danish strains of Staphylococcus aureus isolated from cases of bacteriaemia. Journal of Medical Microbiology, 13, 383–391.

    Article  CAS  Google Scholar 

  • Rosenberg, J., Jarvis, W. R., Abbott, S. L., & Vugia D. J. (2004). Emergence of vancomycin-resistant enterococci in San Francisco Bay area hospitals during 1994 to 1998. Infection Control and Hospital Epidemiology, 25(5), 408–412.

    Article  Google Scholar 

  • Ruof, K. L., de la Maza, L., Murtagh, M. J., Spargo, J. D., & Ferraro, M. J. (1990). Species identities of enterococci isolated from clinical specimens. Journal of Clinical Microbiology, 28(3), 435–437.

    Google Scholar 

  • Saliba, L. J., & Helmer, R. (1990). Health risks associated with pollution of coastal bathing waters. World Health Statistics Quarterly, 43(3), 177–187.

    CAS  Google Scholar 

  • Silva, A. A. L. E., & Hofer, E. (1993). Resistance to antibiotics and heavy metals in Escherichia coli from marine fish, environmental toxicology and water quality. Environmental Toxicology and Water Quality, 8, 1–11.

    Article  Google Scholar 

  • Sjogren, R. E., & Port, J. (1981). Heavy metal-antibiotic resistant bacteria in a lake recreational area. Water, Air, and Soil Pollution, 15, 29–44.

    Article  Google Scholar 

  • Stiefel, U., Paterson, D. L., Pultz, N. J., Gordon, S. M., Aron, D. C., & Donskey C. J. (2004). Effect of the increasing use of piperacillin/tazobactam on the incidence of vancomycin-resistant enterococci in four academic medical centers. Infection Control and Hospital Epidemiology, 25(5) 380–383.

    Article  Google Scholar 

  • Von Schirnding, Y. E., Kfir, R., Cabelli, V., Franklin, L., & Joubert, G. (1992). Morbidity among bathers exposed to polluted seawater. A prospective epidemiological study. South African Medical Journal, 81(11), 543–546.

    Google Scholar 

  • Washington, J. A., & Sutter, V. L. (1981). Dilution test procedures. In E. H. Lennette, A. Balows, W. J. Hausler, & J. P. Truant (Eds.), Manual of clinical microbiology (pp. 549–555). Washington, District of Columbia: American Society for Microbiology.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ayten Kimiran-Erdem.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kimiran-Erdem, A., Arslan, E.O., Sanli Yurudu, N.O. et al. Isolation and Identification of Enterococci from Seawater Samples: Assessment of Their Resistance to Antibiotics and Heavy Metals. Environ Monit Assess 125, 219–228 (2007). https://doi.org/10.1007/s10661-006-9506-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10661-006-9506-0

Keywords

Navigation