Heavy Metals and Antibiotic Resistant Bacteria in Green Turtles are Indicators of Environmental Pollution

Authors: S. K. Al-Musharafi, I. Y. Mahmoud, S. N. Al-Bahry

Abstract:

Freshly laid eggs from green turtles, Chelonia mydas, were randomly collected from Ras Al-Hadd Reserve, Oman. Eggshells taken from eggs and sand collected from the body chamber were analyzed for eight heavy metals (Al, Br, Cd, Co, Cu, Fe, S, and Zn) using inductively coupled plasma mass spectrometry (ICP). Heavy metal concentrations varied significantly (P<0.05) between nest sand and eggshells. Zn values were significantly higher than the other heavy metals. A total of 60 heterotrophic bacteria belong to eight genera were isolated from fresh egg contents (albumen and yolk). Resistance of the isolates to Ak = amikacin, Ak = amikacin, Amp= ampicillin, Gm= gentamycin, Cn = chloramphenicol, Min = minocycline, N = Neomycin, S= streptomycin, Smx = sulphamethoxazole, Tmp = trimethoprim, Tob = tobramycin was tested. More than 40% of the isolates were multiple resistant to 2-10 antibiotics. Most of the resistant strains were also resistant to Zn. The value of these findings may indicate that the origin of pollution is of human contaminated effluents.

Keywords: Antibiotic resistance, bacteria, environment, heavy metals, sea turtles.

Digital Object Identifier (DOI): doi.org/10.5281/zenodo.1100569

References:

[1] SN Al-Bahry, IY Mahmoud, AE Elshafie, A Al-Harthy, S Al-Ghafri, I Al-Amri and AY Alkindi. Bacterial flora and antibiotic resistance from eggs of green turtles Chelonia mydas: an indication of polluted effluents. Marine Poll Bull. 41, pp. 214-221. 2009a
[2] SN Al-Bahry, Mahmoud, S Al-Rawahi and J Paulson. Egg contamination as an indicator of environmental health. In: Impact of Egg Contamination on Environmental Health. Nova Science Publisher Inc. New York. 2011a.
[3] SN Al-Bahry, MA Al-Zadjali, IY Mahmoud and AE Elshafie. Biomonitoring marine habitats in reference to antibiotic resistant bacteria and ampicillin resistance determinants from oviductal fluid of the nesting green sea turtle, Chelonia mydas. Chemosphere. 87, pp. 1308-1315. 2012.
[4] SK Al-Musharafi. Analysis of heavy metal in eggshells of green turtles, Chelonia mydas, by scanning electron microscopy and x-ray microanalysis. In: Biotechnology and Conservation of Species from Arid Regions. Nova Science Publisher, Inc. New York, USA. p.p. 138-144. 2014.
[5] SH Al-Rawahy, AY Al Kindi, A Elshafie, IY Mahmoud IY, S.N. Al- Bahry, S.S. Al-Siyabi, M.H. Mansour and A.A. Al-Kiyumi, Accumulation of metals in the egg yolk and liver of hatchling of green turtles Chelonia mydas at Ras Al Hadd, Sultanate of Oman. ANSI: J. Biol. Sci. 7, pp. 925-930. 2007.
[6] M Foti, C. Giacopello, T Bottari, V Fisichella, D Rinaldo and C Mamminac. Antibiotic resistance of Gram negatives isolates from loggerhead sea turtles (Caretta caretta) in the central Mediterranean Sea. Mar. Pollut. Bull. 58, pp. 1363-1366. 2009.
[7] SN Al-Bahry, IY Mahmoud, KI Al-Belushi, AE Elshafie, A Al-Harthy and CK Bakheit. Coastal sewage discharge and its impact on fish with reference to antibiotic resistant enteric bacteria and enteric pathogens as bio-indicators of pollution. Chemosphere. 77, p.p. 1534-1539. 2009c
[8] SN Al-Bahry, IY Mahmoud, JR Paulson and SK Al- Musharafi. Antibiotic resistant bacteria in terrestrial and aquatic environments: A review. IAJAA. 4, p.p. 1-11. 2015.
[9] SK, Al-Musharafi Mahmoud IY and Al-Bahry SN. 2013b. Contamination of marine fish by heavy metals from coastal sewage treated effluent runoff. The Third Asian Conference on Sustainability, Energy and the Environment. Osaka, Japan. IAFOR. Pp. 100-107. 2013
[10] Shahidul, and M Tanaka, Impacts of pollution on coastal and marine ecosystems including coastal and marine fisheries and approach for management: a review and synthesis. Marine Poll Bull. 48, pp. 624-649, 2004.
[11] FX Han, A Banin, WL Kingery, GB Triplett, LX, SJ Zhou Zheng and WX Ding. New approach to studies of heavy metal redistribution in soil. Adv Env Res. 8, pp. 113- 120. 2003.
[12] J Kojadinovic, M Potier, CM Le, RP Cosson, and P Bustamante. Bioaccumulation of trace elements in pelagic fish from the Western Indian Ocean. Environ. Pollut. 146, pp. 548-566. 2007.
[13] SN Al-Bahry, IY Mahmoud, A. Al-Khaifi, AE Elshafie and A. Al- Harthy. Viability of multiple antibiotic resistant bacteria in distribution lines of treated sewage effluent used for irrigation. Water Sci Technol. 60, pp. 2939-2948. 2009b.
[14] S Kim and DS Aga. Potential ecological and human health impacts of antibiotics and antibiotic-resistant bacteria from wastewater treatment plants. J Toxicol Environ Health B Crit Rev. 10, pp.559-573. 2007.
[15] Kümmerer K. Antibiotics in the aquatic environment. A review. Part I. Chemosphere 75, 417-434. 2009a.
[16] Kümmerer K. 2009b. Antibiotics in the aquatic environment. A review. Part II. Chemosphere, 75, 435-441. 2009a.
[17] IY Mahmoud, SN Al-Bahry and SK Al-Musharafi. Fresh water habitat pollution by treated sewage effluent in relation to multiple-antibioticresistant bacteria. APCBEES Procedia. 5, pp. 363-367. 2013.
[18] OL Akinbowale, H Peng, P Grant and MD Barton. Antibiotic and heavy metal resistance in motile aeromonads and pseudomonads from rainbow trout (Oncorhynchus mykiss) farms in Australia. Int J Antimicrob Ag. 30, pp. 177-182. 2007.
[19] L Bass, CA Liebert, MD Lee, AO Summers, DG White, SG Thayer and JJ Maurer. Incidence and characterization of integrons, genetic elements mediating multiple-drug resistance in avian Escherichia coli. Antimicrob. Agents Chemother. 43, pp. 2925-2929. 1999.
[20] CS Hölzel, C Müller, KS Harms, S Mikolajewski, S Schäfer, K Schwaiger and J Bauer. Heavy metals in liquid pig manure in light of bacterial antimicrobial resistance. Environ Res. 11, pp. 21-27. 2012.
[21] SK Al-Musharafi, IY Mahmoud and SN Al-Bahry. Environmental contamination by industrial effluents and sludge relative to heavy metals. GEP 2, pp. 14-18. 2014a.
[22] JW, Edwards, KS Edyvane, VA Boxall, M Hamann and KL Soole, Metal levels in seston and marine fish flesh near industrial and metropolitan centres in South Australia. Marine Poll Bull. 42, pp. 389- 396. 2001.
[23] J Burger and M Gochfeld, Cadmium and lead in common terns (Aves: Sterna hirundo): relationship between levels in parents and eggs. Environ. Monit. Assess. 16, pp. 253-258. 1991.
[24] LA Grabowski, JLJ Houpis, WI Woods, and KA Johson, Seasonal bioavailability of sediemt-associated heavy metals along the Mississippi river floodplain. Chemosphere, 25, pp. 643-651. 2001.
[25] CLSI, Clinical Laboratory Standard Institution, Performance Standards for Antimicrobial Susceptibility Testing; 17th Informational Supplement. CLSI M100-S17. CLSI, Wayne, PA. 2007.
[26] SN Al-Bahry, IY Mahmoud, SK Al-Musharafi, IS Al-Gharaibi, NK Al- Harthy, HA Al-Zadjali, Microbial and chemical pollution of water-wells relative to sewage effluents in Oman. IJSEE. 1, pp. 35-56. 2014a.
[27] SK Al-Musharafi, IY Mahmoud and SN Al-Bahry. Heavy metal contamination from treated sewage effluents. 11th International Conference on Modelling, Monitoring and Management of Water Pollution. WIT Transactions on Ecology and The Environment, New Forest. UK. Vol. 164, pp. 381-389. 2012.
[28] SK Al-Musharafi, IY Mahmoud and SN Al-Bahry. Heavy metal pollution from treated sewage effluent. Procedia APCBEES. 5, 344-348. 2013a.
[29] SK, Al-Musharafi, IY, Mahmoud and SN Al-Bahry.. Environmental hazards and pollution from liquid waste lagoons. IPCBEE 69, pp. 1-5. 2014b.
[30] CJ Henry, KF Beal, RB Bury and R Goggans. Organochloride pesticieds, PCB, trace elements and metals in western pond turtle eggs for Oregon. Northwest Sci., 77, 46-53. 2003.
[31] ER Harper, JA St Leger, JA Westberg, L Mazzaro, T Schmitt, TH Reidarson, M Tucker, DH Cross and B Puschner. Tissue heavy metal concentrations of stranded California sea lions (Zalophus californianus) in Southern California. Environ. Pollut. 147, pp. 677-682. 2007.
[32] MM Storelli, G Barone, A Storelli and GO Marcotrigiano. Total and subcellular distribution of trace elements (Cd, Cu and Zn) in the liver and kidney of green turtles (Chelonia mydas) from the Mediterranean Sea. Chemosphere. 70, p. 908-913. 2008.
[33] Berger, MW LeChevallier, DJ Reasoner. Control of biofilm growth in drinking water distribution systems. United States Environmental Protection Agency, Office of Research and Development, Washington D.C. 1992.
[34] JA Tree, RM Adams and DN Less. Chlorination of indicator bacteria and viruses in primary sewage effluent. J. Appl. Microbiol. 69, pp. 2038- 2043. 2003.
[35] R Shrivastava, RK Upreti, SR Jain, KN Prasad, PK Seth and UC Chaturvedi. Suboptimal chlorine treatment of drinking water leads to selection of multidrug-resistant Pseudomonas aeruginosa. Ecotoxicol Environ Safety. 58, pp. 277-283. 2004.
[36] Omani Standards (OS) 52/1 for Wastewater reuse and discharge. Ministry of Environment Decree No 52/1-standards for the minimization of pollution to air, water and soil. Ministry of Environment. Muscat, Oman. 1996.
[37] World Health Organization (WHO). A compendium of standards for wastewater reuse in the Eastern Mediterranean Region. Regional Office for the Eastern Mediterranean. Regional Centre for Environmental Health Activities. 2005.