Skip to main content
Log in

Removal of heavy metals and antibiotics from treated sewage effluent by bacteria

  • Review
  • Published:
Clean Technologies and Environmental Policy Aims and scope Submit manuscript

Abstract

The increased loads of antibiotics and heavy metals in sewage lead to bacterial cells acquiring resistance to both heavy metals and antibiotics. Therefore, these bacteria can play an important role for removal of pollutants from sewage. The utilization of the microbial processes such as biosorption and enzymatic biodegradation processes has increased during the recent years. These processes are significantly inexpensive and eco-friendly. Enzymatic techniques known as white biotechnology have the ability to degrade complex compounds. Hence, these can be applied to industrial processes. In the current review, the removal of heavy metals and antibiotics from treated sewage effluents by heavy metal/antibiotic-resistant bacteria will be discussed.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abdel-Monem MO, Al-Zubeiry AH, AL-Gheethi AAS (2008) Survival of enteric indicators and pathogenic bacteria in sewage sludge after thermal treatment. J Bot Assut Univ Egypt 27:171–183

  • Abdel-Monem MO, Al-Zubeiry AH, Al-Gheethi AA (2010) Biosorption of nickel by Pseudomonas cepacia 120S and Bacillus subtilis 117S. Water Sci Technol 61:2994–3007

    Article  CAS  Google Scholar 

  • Achoka JD (2002) The efficiency of oxidation ponds at the Kraft pulp and Paper mill at Webuye in Kenya. Water Res 36(5):1203–1212

    Article  CAS  Google Scholar 

  • Adenuga AA, Ogunfowokan AO, Torto N, Okoh EK (2007) Levels of Mn, Fe, Ni, Cu, Zn And Cd, in effluent from a sewage treatment oxidation pond and a receiving stream—a preliminary study. IFE J Sci 9:115–128

    Google Scholar 

  • Ahmady-Asbchin S, Bahrami AM (2011) Nickel biosorption by immobilized biomass of Bacillus sp. from aqueous solution. Adv Environ Biol 5:1656–1662

    CAS  Google Scholar 

  • Ajmal M, Rao RAK, Ahmad R, Ahmad J (2000) Adsorption studies on citrus reticulate (fruit peel of orange): removal and recovery of Ni (II) from electroplating wastewater. J Hazard Mater 79:117–131

    Article  CAS  Google Scholar 

  • Akrivos J, Mamais D, Katsara K, Andreadakis AD (2000) Agricultural utilization of lime treated sewage sludge. Water Sci Technol 42:203–210

    CAS  Google Scholar 

  • Aksu Z (2001) Equilibrium and kinetic modelling of cadmium (II) biosorption by Chlorella vulgaris in batch system: effect of temperature. Sep Purif Technol 21:285–294

    Article  CAS  Google Scholar 

  • Aksu Z (2002) Determination of the equilibrium, kinetic and thermodynamic parameters of the batch biosorption of nickel (II) ions on to Chlorella vulgaris. Process Biochem 38:89–99

    Article  CAS  Google Scholar 

  • Aksu Z, Tunc O (2005) Application of biosorption for penicillin G removal: comparison with activated carbon. Process Biochem 40:831–847

    Article  CAS  Google Scholar 

  • Alcalde M, Ferrer M, Plou FJ, Ballesteros A (2006) Environmental biocatalysis: from remediation with enzymes to novel green processes. Trends Biotechnol 24:281–287

    Article  CAS  Google Scholar 

  • Al-Enezi G, Hamoda MF, Fawzi N (2004) Heavy metals content of municipal wastewater and sludges in Kuwait. J Environ Sci Health A 39:397–407

    Article  CAS  Google Scholar 

  • Al-Garni SM (2005) Biosorption of lead by Gram-ve capsulated and non-capsulated bacteria. Water SA 31:12–17

    Google Scholar 

  • Al-Gheethi AAS (2014) Screening of bacterial isolates from sewage treated effluent with potential to remove heavy metals and β-lactam antibiotics. PhD Thesis, Environmental Technology Division, School of Industrial Technology, University Science Malaysia, Penang

  • Al-Gheethi AAS, Norli I (2014) Biodegradation of pharmaceutical wastes in treated sewage effluents by Bacillus subtilis 1556WTNC. Environ Process 1:459–489

    Article  Google Scholar 

  • Al-Gheethi AAS, Norli I, Lalunga J, Azieda T, Efaq AN, Ab Kadir MO (2013) Susceptibility for antibiotics among faecal indicators and pathogenic bacteria in sewage treated effluents. Water Pract Technol 8:1–489

    Article  Google Scholar 

  • Al-Gheethi AAS, Norli I, Lalung J, Megat-Azlan A, Nur-Farehah ZA, Ab. Kadir MO (2014) Biosorption of heavy metals and cephalexin from secondary effluents by tolerant bacteria. Clean Technol Environ Policy 16:137–148. doi:10.1007/s10098-013-0611-9

    Article  CAS  Google Scholar 

  • Alissa EM, Ferns GA (2011) Heavy metal poisoning and cardiovascular disease. J Toxicol 2011:1–21

    Article  CAS  Google Scholar 

  • Al-Musharafi SK, Mahmoud IY, Al-Bahry SN (2013) Heavy metals infiltration from sewage treated effluent into soil and tomato plants. In: 4th International conference on food engineering and biotechnology (IPCBEE), vol 50. IACSIT Press, Singapore

  • Al-Sabahi E, Abdul-Rahim S, Wan-Zuhairi WY, Alshaebi F, Al Nozaily F (2009) Assessment of groundwater and surface water pollution at Mitm Area, Ibb City, Yemen. Am J Appl Sci 6(4):772–783

    Article  Google Scholar 

  • Aminov RI (2009) The role of antibiotics and antibiotic resistance in nature. Environ Microbiol 11:2970–2988

    Article  CAS  Google Scholar 

  • Aravindhan R, Fathima A, Selvamurugan M, Rao JR, Balachandran UN (2012) Adsorption, desorption, and kinetic study on Cr(III) removal from aqueous solution using Bacillus subtilis biomass. Clean Technol Environ Policy 14:727–735. doi:10.1007/s10098-011-0440-7

    Article  CAS  Google Scholar 

  • Arican B, Gokcay CF, Yetis U (2002) Mechanistics of nickel sorption by activated sludge. Process Biochem 37:1307–1315

    Article  CAS  Google Scholar 

  • Atkinson BW, Bux F, Kasan HC (1998) Considerations for application of biosorption technology to remediate metal-contaminated industrial effluents. Water SA 24:129–136

    CAS  Google Scholar 

  • Avisar D, Lester Y, Ronen D (2009) Sulfamethoxazole contamination of a deep phreatic aquifer. Sci Total Environ 407:4278–4282

    Article  CAS  Google Scholar 

  • Bae W, Wu CH, Kostal J, Mulchandani A, Chen W (2003) Enhanced mercury biosorption by bacterial cells with surface- displayed MerR. Appl Environ Microbiol 69:3176–3180

    Article  CAS  Google Scholar 

  • Banik RM, Prakash M (2004) Laundry detergent compatibility of alkaline protease from Bacillus cereus. Microbiol Res 159:135–140

    Article  CAS  Google Scholar 

  • Barbieri M (2008) The mechanisms of evolution: natural selection and natural conventions. Biosemiotics 1:15–35

    Article  Google Scholar 

  • Barceloux DG (1999a) Copper. J Toxicol Clin Toxicol 37:217–230

    Article  CAS  Google Scholar 

  • Barceloux DG (1999b) Nickel. J Toxicol Clin Toxicol 37:239–258

    Article  CAS  Google Scholar 

  • Barnhill AE, Weeks KE, Xiong N, Day TA, Carlson SA (2010) Identification of multiresistant Salmonella isolates capable of subsisting on antibiotics. Appl Environ Microbiol 76:2678–2680

    Article  CAS  Google Scholar 

  • Baryla A, Laborde C, Montillet JL, Triantaphylides C, Chagvardieff P (2000) Evaluation of lipid peroxidation as a toxicity bioassay for plants exposed to copper. Environ Pollut 109:131–135

    Article  CAS  Google Scholar 

  • Batt AL, Kim S, Aga DS (2007) Comparison of the occurrence of antibiotics in four full-scale wastewater treatment plants with varying designs and operations. Chemosphere 68:428–435

    Article  CAS  Google Scholar 

  • Behbahaninia A, Mirbagheri SA, Nouri J (2010) Effects of sludge from wastewater treatment plants on heavy metals transport to soils and groundwater. Iran J Environ Health Sci Eng 7:401–406

    CAS  Google Scholar 

  • Berg J, Tom-Petersen A, Nybroe O (2005) Copper amendment of agricultural soil selects for bacterial antibiotic resistance in the field. Lett Appl Microbiol 40:146–151

    Article  CAS  Google Scholar 

  • Blackwell KJ, Singleton I, Tobin JM (1995) Metal cation uptake by yeast: a review. Appl Microbiol Biotechnol 43:579–584

    Article  CAS  Google Scholar 

  • Brady D, Stoll A, Duncan JR (1994) Biosorption of heavy metals cations by nonviable yeast biomass. Environ Technol 15:429–448

    Article  CAS  Google Scholar 

  • Breierova E, Ingrid V, Vlasta S, Eva S, Miroslav F, Tomas G, Jan S (2002) Biosorption of cadmium ions by different yeast species. Z Naturforch 57:634–639

    CAS  Google Scholar 

  • Brierley CL (1990) Bioremediation of metal-contaminated surface and ground waters. Geomicrobiol J 8:201–233

    Article  CAS  Google Scholar 

  • Budyanto S, Soedjono S, Irawaty W, Indraswati N (2008) Studies of adsorption equilibrium and kinetics of amoxicillin from simulated wastewater using activated carbon and natural bentonite. J Environ Prot Sci 2:72–80

    Google Scholar 

  • Cai-Ming T, Qiu-Xin H, Yi-Yi YU, Xian-Zhi P (2009) Multiresidue determination of sulfonamides, macrolides, trimethoprim, and chloramphenicol in sewage sludge and sediment using ultrasonic extraction coupled with solid phase extraction and liquid chromatography- tandem mass spectrometry. Chin J Anal Chem 37:1119–1124

    Article  Google Scholar 

  • CAST (1976) Application of sewage sludge to cropland appraisal of potential hazards of the heavy metals to plants and animals. EPA Report No. 430/9-76-013. Council for Agricultural Science and Technology, U.S. Environmental Protection Agency, Office of Water Program Operations, Washington

  • CDC (2006) The national antimicrobial resistance monitoring system for enteric bacteria (NARMS): human isolates final report. U.S. Department of Health and Human Services, Centre for Disease Control (CDC), Atlanta

  • Ceribasi IH, Yetis U (2001) Biosorption of Ni(ii) and Pb(ii) by Phanerochaete chrysosporium from a binary metal system kinetics. Water SA 27:14–21

    Google Scholar 

  • Cha JM, Yang S, Carlson KH (2006) Trace determination of β-lactam antibiotics in surface water and urban wastewater using liquid chromatography combined with electrospray tandem mass spectrometry. J Chromatogr A 1115:46–57

    Article  CAS  Google Scholar 

  • Chambers HF (2005) Penicillins. In Mandell GL, Bennett JE, Dolin R (eds) Principles and practice of infectious diseases, 6th ed. Elsevier Churchill Livingstone, London, pp 281–293

    Google Scholar 

  • Chesworth W (1991) Geochemistry of micronutrients. In: Mortvedt JJ, Cox FR, Shuman LM, Welch RM (eds) Micronutrients in agriculture, 2nd edn. Soil Science Society of America, Madison, pp 1–29

    Google Scholar 

  • Cho YJ (2010) Evaluation of degradation of antibiotic tetracycline in pig manure by electron beam irradiation. Bull Environ Contam Toxicol 84:450–453

    Article  CAS  Google Scholar 

  • Chouchene A, Jeguirim M, Trouvé G (2014) Biosorption performance, combustion behavior, and leaching characteristics of olive solid waste during the removal of copper and nickel from aqueous solutions. Clean Technol Environ Policy 16:979–986. doi:10.1007/s10098-013-0680-9

    Article  CAS  Google Scholar 

  • Choudhary S, Goyal V, Singh S (2014) Removal of copper(II) and chromium(VI) from aqueous solution using sorghum roots (S. bicolor): a kinetic and thermodynamic study. Clean Technol Environ Policy (Online). doi:10.1007/s10098-014-0860-2

    Google Scholar 

  • Chua H, Hua FL (1996) Effects of a heavy metal (zinc) on organic adsorption capacity and organic removal in activated sludge. Appl Biochem Biotechnol 57(58):845–849

    Article  Google Scholar 

  • Cogliani C, Goossens H, Greko C (2011) Restricting antimicrobial use in food animals: lessons from Europe. Microbe 6(6):274–279

    Google Scholar 

  • Connor SC, Everett JR, Jennings KR, Nicholson JK, Woodnutt G (1994) High resolution H NMR spectroscopic studies of the metabolism and excretion of ampicillin in rats and amoxicillin in rats and man. J Pharm Pharmacol 46:128–134

    Article  CAS  Google Scholar 

  • Cornforth DM, Foster KR (2013) Competition sensing: the social side of bacterial stress responses. Nat Rev Microbiol 11:285–293

    Article  CAS  Google Scholar 

  • Dalkmann P, Broszat M, Siebe C, Willaschek E, Sakinc T, Huebner H, Amelung W, Grohmann E, Siemens J (2012) Accumulation of pharmaceuticals, Enterococcus, and resistance genes in soils irrigated with wastewater for zero to 100 years in Central Mexico. PLoS ONE 7:e45397. doi:10.1371/journal.pone.0045397

    Article  CAS  Google Scholar 

  • Davies J, Davies D (2010) Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74:417–433

    Article  CAS  Google Scholar 

  • Deshpande AD, Baheti KG, Chatterjee NR (2004) Degradation of β-lactam antibiotics. Curr Sci 87:1684–1695

    CAS  Google Scholar 

  • Dimitrova SV (1996) Metal sorption on blast-furnace slag. Water Res 30:228–232

    Article  CAS  Google Scholar 

  • Dionisio F, Matic I, Radman M, Rodrigues OR, Taddei F (2002) Plasmids spread very fast in heterogeneous bacterial communities. Genetics 162:1525–1532

    CAS  Google Scholar 

  • Dixon NE, Gazzola C, Blakeley RL, Zerner B (1975) Jack bean urease (EC 3.5.1.5): a metalloenzyme a simple biological role for nickel. J Am Chem Soc 97:4131–4133

    Article  CAS  Google Scholar 

  • Dodd MC, Buffle MO, von Gunten U (2006) Oxidation of antibacterial molecules by aqueous ozone: moiety-specific reaction kinetics and application to ozone-based wastewater treatment. Environ Sci Technol 40:1969–1977

    Article  CAS  Google Scholar 

  • Doran JL, Leskiw BK, Aippersbach S, Jensen SE (1990) Isolation and characterization of a β-lactamase inhibitory protein from Streptomyces clavuligerus and cloning and analysis of the corresponding gene. J Bacteriol 172:4909–4918

    CAS  Google Scholar 

  • Dosanjh N, Michel SLJ (2006) Microbial nickel metalloregulation NikRs for nickel ions. Curr Opin Chem Biol 10:123–130

    Article  CAS  Google Scholar 

  • Dutta M, Dutta NN, Bhattacharya KG (1999) Aqueous phase adsorption of certain beta-lactam antibiotics onto polymeric resins and activated carbon. Sep Purif Technol 16:213–224

    Article  CAS  Google Scholar 

  • Epstein E (2002) Health issues related to beneficial use of biosolids. In: 16th Annual residuals and biosolids management conference of the Water Environment Federation, Texas, p 9

  • Fagan MJ, Saier MHJ (1994) P-type ATPases of eukaryotes and bacteria: sequence comparisons and construction of phylogenetic trees. J Mol Evol 38:57–99

    Article  CAS  Google Scholar 

  • Fakorede CN, Igbeneghu OA, Odeyemi O (2013) The microbiological and physicochemical characterization of wastewater from a brewery in southwest Nigeria: a case study. Biol Sci Pharm Res 1:1–7

    Google Scholar 

  • FAO (1985) Water quality for agriculture, irrigation and drainage. Food and Agriculture Organization. Paper 29, Rev 1

  • Fath MJ, Kolter R (1993) ABC-transporters: the bacterial exporters. Microbiol Rev 57:995–1017

    CAS  Google Scholar 

  • Fathima A, Aravindhan R, Rao JR, Nair BN (2014) Biomass of Termitomyces clypeatus for chromium(III) removal from chrome tanning wastewater. Clean Technol Environ Policy (Online). doi:10.1007/s10098-014-0799-3

  • Filali BK, Taoufik J, Zeroual Y, Dzairi FZ, Talbi M, Blaghen M (2000) Waste water bacterial isolates resistant to heavy metals and antibiotics. Curr Microbiol 41:151–156

    Article  CAS  Google Scholar 

  • Foo LPY, Tee CZ, Raimy NR, Hassell DG, Lee LY (2012) Potential Malaysia agricultural waste materials for the biosorption of cadmium(II) from aqueous solution. Clean Technol Environ Policy 14:273–280. doi:10.1007/s10098-011-0398-5

    Article  CAS  Google Scholar 

  • French GL (2006) Bactericidal agents in the treatment of MRSA infections the potential role of daptomycin. J Antimicrob Chemother 58:1107–1117

    Article  CAS  Google Scholar 

  • Gaber SE, Rizk MS, Yehia MM (2011) Extraction of certain heavy metals from sewage sludge using different types of acids. J Biochem 23:41–48

    Google Scholar 

  • Gadd GM (1988) Accumulation of metals by microorganisms and algae. In: Rem J, Reed G (eds) Biotechnology—a comprehensive treatise. VCH Publishers, Weinheim, pp 401–403

    Google Scholar 

  • Gadd GM (1990) Heavy metal accumulation by bacteria and other microorganisms. Experientia 46:834–839

    Article  CAS  Google Scholar 

  • Gadd GM (1992) Microbial control of heavy metal pollution. In: Fry JC, Gadd GM, Herbert RA, Jones CW, Watson-Craik A (eds) Microbiology control of pollution. Cambridge University Press

    Google Scholar 

  • Gao L, Shi Y, Li W, Niu H, Liu J, Cai Y (2012) Occurrence of antibiotics in eight sewage treatment plants in Beijing, China. Chemosphere 86:665–671

    Article  CAS  Google Scholar 

  • Garcia-Armisen T, Vercammen K, Passerat J, Triest D, Servais P, Cornelis P (2011) Antimicrobial resistance of heterotrophic bacteria in sewage-contaminated rivers. Water Res 45:788–796

    Article  CAS  Google Scholar 

  • Gerardi MH (2003) The microbiology of anaerobic digesters. Wiley, Hoboken, pp 91–118

    Book  Google Scholar 

  • Giger W, Alder AC, Golet EM, Kohler HE, McArdell CS, Molnar M, Siegrist H, Suter MJ (2003) Occurrence and fate of antibiotics as trace contaminants in wastewaters, sewage sludges, and surface waters. Chimia 57:485–491

    Article  CAS  Google Scholar 

  • Gillespie SH, McHugh TD (2010) Antibiotic resistance protocols, 2nd edn. Springer, New York

    Book  Google Scholar 

  • Gilsdorf JR, Zilinskas RA (2005) New considerations in infectious disease outbreaks: the threat of genetically modified microbes. Clin Infect Dis 40:1160–1165

    Article  Google Scholar 

  • Gobel A, Thomsen A, McArdell CS, Joss A, Giger W (2005) Occurrence and sorption behaviour of sulfonamides, macrolides, and trimethoprim in activated sludge treatment. J Environ Sci Technol 39:3981–3989

    Article  CAS  Google Scholar 

  • Gourdon R, Bhende S, Rus E, Sofer SS (1990) Comparison of cadmium biosorption by Gram-positive and Gram-negative bacteria from activated sludge. Biotechnol Lett 12:839–842

    Article  CAS  Google Scholar 

  • Guilfoile PG (2007) Antibiotic-resistant bacteria. Chelsea House/An imprint of Infobase Publish, New York

  • Gulkowska A, Leung HW, So MK, Taniyasu S, Yamashita N, Yeung L, Richardson BG, Lei AP, Giesy JP, Lam KS (2008) Removal of antibiotics from wastewater by sewage treatment facilities in Hong Kong and Shenzhen, China. Water Res 42:395–403

    Article  CAS  Google Scholar 

  • Guo W, Wang H, Shi Y, Zhang G (2010) Sonochemical degradation of the antibiotic cephalexin in aqueous solution. Water SA 36:651–654

    Article  CAS  Google Scholar 

  • Gutnick DL, Bach H (2000) Engineering bacterial polymers of biosorption of heavy metals: new products and novel formulation. Appl Environ Biotechnol 54:451–460

    Article  CAS  Google Scholar 

  • Habib-ur-Rehman SM, Ahmad I, Shah S (2006) Sorption studies of nickel ions onto saw dust of Dalbergia sissoo. J Chin Chem Soc 53:1045–1052

    Article  CAS  Google Scholar 

  • Haines AS, Jones K, Batt SM, Kosheleva IA, Thomas CM (2007) Sequence of plasmid pBS228 and reconstruction of the IncCP-1alpha phylogeny. Plasmid 58:76–83

    Article  CAS  Google Scholar 

  • Hajar M (2009) Biosorption of cadmium from aqueous solution using dead biomass of brown alga Sargassum sp. Chem Eng Trans 17:1173–1178

    Google Scholar 

  • Handal T, Olsen T (2000) Antimicrobial resistance with focus on oral beta-lactamases. Eur J Oral 108(3):163–174

    Article  CAS  Google Scholar 

  • Hasan SH, Srivastava P (2011) Biosorptive abatement of Cd2+ by water using immobilized biomass of Arthrobacter sp. Response surface methodological approach. Ind Eng Chem Res 50(1):247–258

    Article  CAS  Google Scholar 

  • He ZL, Yang XE, Stoffella PJ (2005) Trace elements in agroecosystems and impacts on the environment. J Trace Elem Med Biol 19:125–140

    Article  CAS  Google Scholar 

  • Hernandez A, Rafael P, Jose M, Martinez L (1998) Metal accumulation and vanadium-induced multidrug resistance by environmental isolates of Escherichia hermannii and Enterobacter cloacae. Appl Environ Microbiol 64:4317–4320

    CAS  Google Scholar 

  • Hong C, Ying HU, Le Zheng W, Bing SHAO (2008) Occurrence of sulfonamide antibiotics in sewage treatment plants. Chin Sci Bull 53:514–520

    Article  CAS  Google Scholar 

  • Hopkins SP, Hames CAC (1994) Zinc, among a ‘cocktail’ of metal pollutants, is responsible for the absence of the terrestrial isopod Porcelio scaber from the vicinity of a primary smelting works. Ecotoxicology 2:68–78

    Article  Google Scholar 

  • Hussein H, Ibrahim SF, Kandeel K, Moawad H (2004) Biosorption of heavy metals from wastewater using Pseudomonas sp. Electron J Biotechnol 7:38–44

    Article  Google Scholar 

  • Ilhan S, Cabuk A, Filik K, Caliskan F (2004) Effect of pre-treatment on biosorption of heavy metals by fungal biomass. Trakya Univ J Sci 5:11–17

    Google Scholar 

  • Jackson VA, Paulse AN, Odendaal JP, Khan S, Khan W (2012) Identification of metal-tolerant organisms isolated from the Plankenburg river, western Cape, South Africa. Water SA 38:29–38

    Article  CAS  Google Scholar 

  • Jafari M, Aghamiri SF, Khaghanic G (2011) Batch adsorption of cephalosporins antibiotics from aqueous solution by means of multi-walled carbon nanotubes. World Appl Sci J 14:1642–1650

    CAS  Google Scholar 

  • Ji X, Shen Q, Liu F, Ma J, Xu G, Wang Y, Wu M (2012) Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai; China. J Hazard Mater 15:178–185

    Article  CAS  Google Scholar 

  • Joss A, Siegrist H, Ternes TA (2008) Are we about to upgrade wastewater treatment for removing organic micropollutants? Water Sci Technol 57:251–255

    Article  CAS  Google Scholar 

  • Jury KL, Vancov T, Stuetz RM, Khan SJ (2010) Antibiotic resistance dissemination and sewage treatment plants. In: Mendez–Vilas A (ed) Current research technology and education topics in applied microbiology and microbial biotechnology. Formatex, Badajoz, pp 509–519

    Google Scholar 

  • Kadirvelu K, Goal J (2007) Eco-friendly technologies for removal of hazardous heavy metals from water and industrial wastewater. In: Allison A (ed) Hazardous materials and wastewater. Nova Science Publishers, Lewinsky, pp 127–148

    Google Scholar 

  • Kaewchai S, Prasertsan P (2002) Biosorption of heavy metal by thermotolerant polymer-producing bacterial cells and the bioflocculant. Songklanakarin J Sci Technol 24:421–430

    CAS  Google Scholar 

  • Karam J, Nicell JA (1997) Potential applications of enzymes in waste treatment. J Chem Tech Biotechnol 69:141–153

    Article  CAS  Google Scholar 

  • Karthikeyan KG, Meyer MT (2006) Occurrence of antibiotics in wastewater treatment facilities in Wisconsin, USA. Sci Total Environ 361:196–207

    Article  CAS  Google Scholar 

  • Kaye KS, Engemann JJ, Fraimow HS, Abrutyn E (2004) Pathogens resistant to antimicrobial agents: epidemiology, molecular mechanisms, and clinical management. Infect Dis Clin N Am 18:467–511

    Article  Google Scholar 

  • Keen OG, Linden KG (2013) Degradation of antibiotic activity during UV/H2O2 advanced oxidation and photolysis in wastewater effluent. Environ Sci Technol 47:13020–13030

    Article  CAS  Google Scholar 

  • Khalikova E, Susi P, Korpela T (2005) Microbial dextran-hydrolyzing enzymes: fundamentals and applications. Microbiol Mol Biol Rev 69:306–325

    Article  CAS  Google Scholar 

  • Khan M, Scullion J (2002) Effect of metal (Cd, Cu, Ni, Pb and Zn) enrichment of sewage sludge on soil microorganisms and their activities. Appl Soil Ecol 20:145–155

    Article  Google Scholar 

  • Kihampa C (2014) β-Lactams and fluoroquinolone antibiotics in influents and effluents of wastewater treatment plants, Dares Salaam, Tanzania. Res J Chem Sci 4:31–36

    CAS  Google Scholar 

  • Kim S, Yun Z, Ha UH, Lee S, Park H, Kwon EE, Cho Y, Choung S, Oh J, Medriano CA, Chandran K (2014) Transfer of antibiotic resistance plasmids in pure and activated sludge cultures in the presence of environmentally representative micro-contaminant concentrations. Sci Total Environ 15:813–820

    Article  CAS  Google Scholar 

  • Kool M (2006) Mathematical model for antibiotic distribution and eradication of bacteria causing Endocarditis. MSc Thesis, University of Twente, the Netherlands, Department of Applied Mathematics, Group of Applied Analysis and Mathematical Physics

  • Kulbat E, Olańczuk-Neyman K, Quant B, Geneja M, Haustein E (2003) Heavy metals removal in the mechanical–biological wastewater treatment plant “Wschód” in Gdańsk. Pol J Environ Stud 12:635–641

    CAS  Google Scholar 

  • Kummerer K (2003) Significance of antibiotics in the environment. J Antimicrob Chemother 52:5–7

    Article  CAS  Google Scholar 

  • Kuroda K, Ueda M (2003) Bioadsorption of cadmium ion by cell surface-engineered yeasts displaying metallo-thionein and hexa His. Appl Microbiol Biotechnol 63:182–186

    Article  CAS  Google Scholar 

  • Kuroda K, Ueda M, Shibasaki S, Tanaka A (2002) Cell surface-engineered yeast with ability to bind, and self-aggregate in response to copper ion. Appl Microbiol Biotechnol 59:259–264

    Article  CAS  Google Scholar 

  • Lajeunesse A, Blais M, Barbeau B, Sauvé S, Gagnon C (2013) Ozone oxidation of antidepressants in wastewater-treatment evaluation and characterization of new by-products by LC-QToFMS. Chem Cent J 7:1–15

    Article  CAS  Google Scholar 

  • Lao-Luque G, Solé M, Gamisans X, Valderrama V, Dorado AD (2014) Characterization of chromium (III) removal from aqueous solutions by an immature coal (leonardite). Toward a better understanding of the phenomena involved. Clean Technol Environ Policy 16:127–136. doi:10.1007/s10098-013-0610-x

    Article  CAS  Google Scholar 

  • Laroche E, Pawlak B, Berthe T, Skurnik D, Petit F (2009) Occurrence of antibiotic resistance and class 1, 2 and 3 integrons in E. coli isolated from a densely populated estuary (Seine, France). FEMS Microbiol Ecol 68:118–130

    Article  CAS  Google Scholar 

  • Lawlor K, Chaudri AM, McGrath SP, Hirsch RR (1999) Gene transfer in bacteria from soils contaminated with heavy metals. Lett Appl Microbiol 28:317–320

    Article  CAS  Google Scholar 

  • Lazăr V, Cernat R, Balotescu C, Cotar A, Coipan E, Cojocaru C (2002) Correlation between multiple antibiotic resistance and heavy-metal tolerance among some E. coli strains isolated from polluted waters. Bacteriol Virus Parazitol Epidemiol 47:155–160

    Google Scholar 

  • Leung WC, Chua H, Lo W (2001) Biosorption of heavy metals by bacteria isolated from activated sludge. Appl Biochem Biotechnol 91–93:171–184

    Article  Google Scholar 

  • Levy SB (1992) Active efflux mechanisms for antimicrobial resistance. Antimicrob Agents Chemother 36:695–703

    Article  CAS  Google Scholar 

  • Lewis K (2007) Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5:48–56

    Article  CAS  Google Scholar 

  • Lewis K (2008) Multidrug tolerance of biofilms and persister cells. In: Romeo T (ed) Bacterial biofilms. Current topics in microbiology and immunology, vol 322. Springer, Heidelberg, pp 107–131

    Google Scholar 

  • Lewis K (2010) Persister cells. Annu Rev Microbiol 64:357–372

    Article  CAS  Google Scholar 

  • Lewis K (2013) Platforms for antibiotic discovery. Nat Rev Drug Dis 12:371–387

    Article  CAS  Google Scholar 

  • Li B, Zhang T (2010) Biodegradation and adsorption of antibiotics in the activated sludge process. J Environ Sci Technol 44:3468–3473

    Article  CAS  Google Scholar 

  • Li JX, Gao J, Luo X, Guo Y (2010) Functions of Bacillus subtilis BS7.29 in wastewater treatment. In: International conference on digital manufacturing and automation (ICDMA) 18–20(1) December 2010, pp 753–756

  • Li W, Shi Y, Gao L, Liu J, Cai Y (2013) Occurrence, distribution and potential affecting factors of antibiotics in sewage sludge of wastewater treatment plants in China. Sci Total Environ 15:306–313

    Article  CAS  Google Scholar 

  • Liang S (2011) Removal of antibiotics from wastewater by adsorption and biodegradation. PhD Thesis, School of Civil & Environmental Engineering. Singapore

  • Liao W, Jiang J, Xu Y, Yi J, Chen T, Su X, Pan S, Wei X, Li Y (2010) Survey for β-lactamase among bacterial isolates from Guangzhou, China hospitals between, 2005–2006. J Antibiot 63:225–229

    Article  CAS  Google Scholar 

  • Lin A, Biyela PT (2005) Convergent acquisition of antibiotic resistance determinants amongst the Enterobacteriaceae isolates of the Mhlathuze River, KwaZulu-Natal (RSA). Water SA 31:250–260

    Google Scholar 

  • Lin AYC, Yu TH, Lateef SK (2009) Removal of pharmaceuticals in secondary wastewater treatment processes in Taiwan. J Hazard Mat 167:1163–1169

    Article  CAS  Google Scholar 

  • Lisa M, Hemmingsen L, Vila AJ (2010) Catalytic role of the metal ion in the metallo-β-lactamase GOB. J Biol Chem 285:4570–4577

    Article  CAS  Google Scholar 

  • Liu HL, Chen BY, Lan YW, Cheng YC (2004) Biosorption of Zn(II) and Cu(II) by the indigenous Thiobacillus thiooxidans. Chem Eng J 97:195–201

    Article  CAS  Google Scholar 

  • Livermore DM (1998) β-Lactamase-mediated resistance and opportunities for its control. J Antimicrob Chemother 41:25–41

    Article  CAS  Google Scholar 

  • Livermore DM, Brown DFG (2001) Detection of β-lactamase mediated resistance. J Antimicrob Chemother 48:59–64

    Article  CAS  Google Scholar 

  • LiW Shi Y, Gao L, Liu J, Cai Y (2013) Occurrence and removal of antibiotics in a municipal wastewater reclamation plant in Beijing, China. Chemosphere 92:435–444

    Article  CAS  Google Scholar 

  • Lo W, Chua H, Lam KH, Bi SP (1999) A comparative investigation on the biosorption of lead by filamentous fungal biomass. Chemosphere 39:2723–2736

    Article  CAS  Google Scholar 

  • Luczkiewicz A, Jankowska K, Bray R, Kulbat E, Quant B, Sokolowska A, Olanczuk-Neyman K (2011) Antimicrobial resistance of faecal indicators in disinfected wastewater. Water Sci Technol 64:2352–2361

    Article  CAS  Google Scholar 

  • Madacha V, Apiratikul R, Pavasant P (2006) Heavy metals uptake by dried Caulerpa lentillifera. In: The 2nd Joint international conference on “Sustainable Energy and Environment (SEE 2006)” E-043 (P), 21–23 November 2006, Bangkok

  • Mahamadia C, Torto N (2007) A comparative study of the kinetic of the nickel biosorption by river green alga obtained from different environments: mine effluent drained drainage and natural river system. Electron J Environ Agric Food Chem 6:2165–2172

    Google Scholar 

  • Mainous AG, Pomeroy C (2001) Management of antimicrobials in infectious diseases. Impact of antibiotic resistance. Humana Press, Totowa

    Book  Google Scholar 

  • Maki T, Hasegawa H, Kitami H, Fumoto K, Munekage Y, Ueda K (2006) Bacterial degradation of antibiotic residues in marine fish farm sediments of Uranouchi Bay and phylogenetic analysis of antibiotic-degrading bacteria using 16S rDNA sequences. Fish Sci 72:811–820

    Article  CAS  Google Scholar 

  • Malik P, Terry TD, Bellintani F, Perham RN (1998) Factors limiting display of foreign peptides on the major coat protein of filamentous bacteriophage capsids and a potential role for leader peptidase. FEBS Lett 436:263–266

    Article  CAS  Google Scholar 

  • Marques AM, Roca X, Simon-Pujol MD, Fuste MC, Congregado F (1991) Uranium accumulation by Pseudomonas sp. EPS 5028. Appl Microbiol Biotechnol 35:406–410

    CAS  Google Scholar 

  • Mcardell CO, Molnar E, Suter MJ, Giger W (2003) Occurrence and fate of macrolide antibiotics in wastewater treatment plants and in the Glatt Valley Watershed, Switzerland. Environ Sci Technol 37:5479–5486

    Article  CAS  Google Scholar 

  • McLaren RG, Smith CJ (1996) Issues in the disposal of industrial and urban wastes. In: Naidu R (ed) Contaminants and the soil environment in the Australasia Pacific Region. Kluwer, Dordrecht, pp 138–212

    Google Scholar 

  • Merrikhpour H, Jalali M (2012) Waste calcite sludge as an adsorbent for the removal of cadmium, copper, lead, and zinc from aqueous solutions. Clean Technol Environ Policy 14:845–855. doi:10.1007/s10098-012-0450-0

    Article  CAS  Google Scholar 

  • Miller ER, Lei X, Ullrey DE (1991) Trace elements in animal nutrition. In: Mortvedt JJ, Cox FR, Shuman LM, Welch RM (eds) Micronutrients in agriculture, 2nd edn. Soil Science Society of America, Madison, pp 593–662

    Google Scholar 

  • Mishra V (2014) Biosorption of zinc ion: a deep comprehension. Appl Water Sci 4:311–332

    Article  CAS  Google Scholar 

  • Mishra V, Tadepalli S (2014) Biosorption of toxic heavy metals on sawdust. CLEAN Soil Air Water (Online). doi:10.1002/clen.201300934

  • Mishra V, Balomajumder C, Agarwal VC (2010a) Zn(II) ion biosorption onto surface of eucalyptus leaf biomass: isotherm, kinetic, and mechanistic modelling. CLEAN Soil Air Water 38:1062–1073

    Article  CAS  Google Scholar 

  • Mishra V, Balomajumder C, Agarwal VC (2010b) Biosorption of Zn (II) onto the surface of non-living biomasses: a comparative study of adsorbent particle size and removal capacity of three different biomasses. Water Air Soil Poll 211:489–500

    Article  CAS  Google Scholar 

  • Mishra V, Balomajumder C, Agarwal VK (2012a) Kinetics, mechanistic and thermodynamics of Zn (II) ion sorption: a modeling approach. CLEAN Soil Air Water 40:718–727

    Article  CAS  Google Scholar 

  • Mishra V, Majumder CB, Agarwal VK (2012b) Sorption of Zn (II) ion onto surface of activated carbon derived from eucalyptus bark saw dust from industrial wastewater: isotherm, kinetics, mechanistic modeling and thermodynamics. Des Water Treat 46:332–352

    Article  CAS  Google Scholar 

  • Mishra V, Balomajumder C, Agarwal VK (2013a) Adsorption of Cu (II) on the surface of non-conventional biomass: a study on forced convective mass transfer in packed bed column. J Waste Manag 2013:1–8

    Article  CAS  Google Scholar 

  • Mishra V, Dalal S, Balomajumder C (2013b) Optimization of physical parameters for batch mode Zn (II) ion removal from liquid phase: a potential biosorption study. Environ Prog Sustain Energy 32:213–222

    Article  CAS  Google Scholar 

  • Mishra V, Balomajumder C, Agarwal VC (2014) Biological removal of heavy metal zinc from industrial effluent by Zinc sequestering bacterium VMSDCM. Clean Technol Environ Policy 16:555–568. doi:10.1007/s10098-013-0655-x

    Article  CAS  Google Scholar 

  • Morikawa M (2006) Beneficial biofilm formation by industrial bacteria Bacillus subtilis and related species. J Biosci Bioeng 101:1–8

    Article  CAS  Google Scholar 

  • Morse A, Jackson A (2003) Fate of a representative pharmaceutical in the environment. Final Report submitted to Texas Water Resources Institute. Texas Tech University, Texas

  • Mulrooney SB, Hausinger RP (2003) Nickel uptake and utilization by microorganisms. FEMS Microbiol Rev 27:239–261

    Article  CAS  Google Scholar 

  • Mussarat M, Bhatti AU, Khan FU (2007) Concentration of metals in sewage and canal water used for irrigation in Peshawar. Sarhad J Agric 23:335–338

    Google Scholar 

  • Muyssen BTA, Brix KV, Deforest DK, Janssen CR (2004) Nickel essentiality and homoeostasis in aquatic organisms. J Environ Rev 12:113–131

    Article  CAS  Google Scholar 

  • Naik UC, Srivastava S, Thakur IS (2012) Isolation and characterization of B. cereus IST105 from electroplating effluent for detoxification of hexavalent chromium. Environ Sci Pollut Res 19:3005–3014

    Article  CAS  Google Scholar 

  • Nanda M, Sharma D, Kumar A (2011) Removal of heavy metals from industrial effluent using bacteria. Int J Environ Sci 2:781–787

    CAS  Google Scholar 

  • Nasr SM, Okbah MA, Kasem SM (2006) Environmental assessment of heavy metal pollution in bottom sediments of Aden Port, Yemen. Int J Oceans Oceanogr 1:99–109

    CAS  Google Scholar 

  • Nasrazadani A, Tahmourespour A, Hoodaji M (2011) Determination of bacteria resistance threshold to lead, zinc and cadmium in three industrial wastewater samples. J Environ Stud 36:75–86

    CAS  Google Scholar 

  • Navarro PG, Blazquez IH, Osso BQ, Martinez PJ, Puentedura MI, Garcia AA (2003) Penicillin degradation catalysed by Zn(II) ions in methanol. Int J Biol Macromol 33:159–166

    Article  CAS  Google Scholar 

  • Nies DH (1999) Microbial heavy metals resistance. Appl Microbiol Biotechnol 51:730–750

    Article  CAS  Google Scholar 

  • Nies DH, Silver S (1995) Ion efflux systems involved in bacterial metal resistances. J Ind Microbiol 14:186–199

    Article  CAS  Google Scholar 

  • Nies DH, Koch S, Wachi S, Peitzsch N, Saier MHJ (1998) CHR, a novel family of prokaryotic proton motive force-driven transporters probably containing chromate/sulfate transporters. J Bacteriol 180:5799–5802

    CAS  Google Scholar 

  • Nikaido H, Rosenberg EY (1983) Porin channels in E. coli: studies with liposomes reconstituted from purified proteins. J Bacteriol 153:241–252

    CAS  Google Scholar 

  • Nitzan Y, Deutsch EB, Pechatnikov I (2002) Diffusion of β-lactam antibiotics through oligomeric or monomeric porin channels of some Gram-negative bacteria. Curr Microbiol 45(6):446–455

    Article  CAS  Google Scholar 

  • Nizet V (2006) Antimicrobial peptide resistance mechanisms of human bacterial pathogens. Curr Issues Mol Biol 8:11–26

    CAS  Google Scholar 

  • Nuhoglu Y, Ogoz E (2003) Removal of copper (II) from aqueous solutions by adsorption on the cone biomass of Thuja orientalis. Process Biochem 38:1047–1061

    Article  CAS  Google Scholar 

  • Ogunfowokan AO, Adegnuga AA, Torto N, Okoh EK (2008) Heavy metals pollution in a sewage treatment oxidation pond and the receiving stream of the Obafemi Awolowo University, Ile Ife, Nigeria. Environ Monit Assess 143:25–41

    Article  CAS  Google Scholar 

  • Oliveira AS, Bocio A, Trevilato TM, Takayanagui AM, Domingo JL, Segura-Muñoz SI (2007) Heavy metals in untreated/treated urban effluent and sludge from a biological wastewater treatment plant. Environ Sci Pollut Res Int 14:483–439

    Article  CAS  Google Scholar 

  • Olofsson U (2004) Fate of human antibiotics during sewage water treatment. Environmental Chemistry, Umeå University and Per Rendahl at UMEVA

  • Ozturk S, Aslim B, Tunceli A (2011) Biosorption of chromium(VI) ions from aqueous system by free and immobilized biomass of wild Synechocystis sp.: a comparative study. Fresenius Environ Bull 20:2412–2418

    CAS  Google Scholar 

  • Padmavathy V, Vasudevan P, Dhingra SC (2003) Biosorption of nickel (II) ions on Baker’s yeast. Process Biochem 38:1389–1395

    Article  CAS  Google Scholar 

  • Park H, Choung Y (2007) Degradation of antibiotics (tetracycline, sulfathiazole, ampicillin) using enzymes of Glutathion S-transferase. Hum Ecol Risk Assess 13:1147–1155

    Article  CAS  Google Scholar 

  • Paulsen IT, Saier MH (1997) A novel family of ubiquitous heavy metal ion transport proteins. J Membr Biol 156:99–103

    Article  CAS  Google Scholar 

  • Paulsen IT, Sliwinski MK, Nelissen B, Goffeau A, Saier MH (1998) Unified inventory of established and putative transporters encoded within the complete genome of Saccharomyces cerevisiae. FEBS Lett 430:116–125

    Article  CAS  Google Scholar 

  • Pauwels B, Verstraete W (2006) The treatment of hospital wastewater: an appraisal. J Water Health 4:405–416

    CAS  Google Scholar 

  • Peltier E, Vincent J, Finn C, Graham DW (2010) Zinc-induced antibiotic resistance in activated sludge bioreactors. Water Res 44:3829–3836

    Article  CAS  Google Scholar 

  • Prado N, Ochoa J, Amrane A (2009) Biodegradation and biosorption of tetracycline and tylosin antibiotics in activated sludge system. Process Biochem 44:1302–1306

    Article  CAS  Google Scholar 

  • Prakash D, Verma S, Bhatia R, Tiwary BN (2011) Risks and precautions of genetically modified organisms. ISRN Ecol 2011:1–13

    Article  Google Scholar 

  • Prescott VE, Campbell PM, Moore A, Mattes J, Rothenberg ME, Foster PS, Higgins TJV, Hogan SP (2005) Transgenic expression of bean α-amylase inhibitor in peas results in altered structure and immunogenicity. J Agric Food Chem 53:9023–9030

    Article  CAS  Google Scholar 

  • Pumpel T, Macaskie LE, Finlay JA, Diels L, Tsezos M (2003) Nickel removal from nickel-plating wastewater using a biologically active moving-bed sand filter. Biotechnol Met 16:567–581

    Google Scholar 

  • Putra EK, Pranowo R, Sunarso J, Indraswati N, Ismadji S (2009) Performance of activated carbon and bentonite for adsorption of amoxicillin from wastewater: mechanisms, isotherms and kinetics. Water Res 43:2419–2430

    Article  CAS  Google Scholar 

  • Qureshi S, Richards BK, Steenhuis TS, McBride MB, Baveye P, Dousset S (2004) Microbial acidication and pH effects on trace element release from sewage sludge. Environ Pollut 132:61–71

    Article  CAS  Google Scholar 

  • Radwan J, Babik W (2012) The genomics of adaptation. Proc R Soc B 279(1749):5024–5028

    Article  Google Scholar 

  • Ragsdale SW (1998) Nickel biochemistry. Curr Opin Chem Biol 2:208–215

    Article  CAS  Google Scholar 

  • Rajbanshi A (2008) Study on heavy metal resistant bacteria in Guheswori Sewage Treatment Plant. Our Nat 6:52–57

    Google Scholar 

  • Rao DG, Senthilkumar R, Byrne A, Feroz S (2012) Wastewater treatment: advanced processes and technologies, chap 13. In: Thanikal JV (ed) Anaerobic fixed bed reactor for treatment of industrial wastewater. CRC Press, Boca Raton, pp 335–354

  • Rasmussen LD, Sørensen SJ (1998) The effect of longterm exposure to mercury on the bacterial community in marine sediment. Curr Microbiol 36:291–297

    Article  CAS  Google Scholar 

  • Rathnayake IVN, Megharaj M, Bolan N, Naidu R (2009) Tolerance of heavy metals by Gram positive soil bacteria. World Acad Sci Eng Technol 29:1050–1054

    Google Scholar 

  • Regine HS, Vieira F, Volesky B (2000) Biosorption: a solution to pollution. Int J Microbiol 3:17–24

    Google Scholar 

  • Robinson PK (1998) Immobilized algal technology for wastewater treatment. In: Wong YS, Tam FY (eds) wastewater treatment with algae. Springer, Berlin, pp 1–16

    Chapter  Google Scholar 

  • Romheld V, Marschner H (1991) Function of micronutrients in plants. In: Mortvedt JJ, Cox FR, Shuman LM, Welch RM (eds) Micronutrients in agriculture, 2nd edn. Soil Science Society of America, Madison, pp 297–328

    Google Scholar 

  • Sa’idi M (2010) Experimental studies on effect of heavy metals presence in industrial wastewater on biological treatment. Int J Environ Sci 1(4):666–676

    Google Scholar 

  • Saier MHJ (1994) Computer-aided analyses of transport protein sequences: gleaning evidence concerning function, structure, biogenesis, and evolution. Microbiol Rev 58:71–93

    CAS  Google Scholar 

  • Saier MH, Tam R, Reizer A, Reizer J (1994) Two novel families of bacterial membrane proteins concerned with nodulation, cell division and transport. Mol Microbiol 11(8):41–847

    Google Scholar 

  • Saniedanesh MH, Wan Alwi SR, Abdul-Manan Z (2013) Potential of heavy metal recovery from wastewater and sewage sludge. In: Proceedings of the 6th International conference on process systems engineering (PSE ASIA), 25–27 June 2013, Kuala Lumpur

  • Scancar J, Milacic R, Strazar M, Burica O (2000) Total metal concentrations and partitioning of Cd, Cr, Cu, Fe, Ni and Zn in sewage sludge. Sci Total Environ 250(1–3):9–19

    Article  CAS  Google Scholar 

  • Selatnia A, Boukazoula A, Kechid N, Bakhti MZ, Chergui A, Kerchich Y (2004) Biosorption of lead (II) from aqueous solution by a bacterial dead Streptomyces rimosus biomass. Biochem Eng J 19(2):127–135

    Article  CAS  Google Scholar 

  • Servais P, Passerat J (2009) Antimicrobial resistance of fecal bacteria in waters of the Seine river watershed (France). J Sci Environ 408(2):365–372

    CAS  Google Scholar 

  • Shakoori AR, Muneer B (2002) Copper-resistant bacteria from industrial effluents and their role in remediation of heavy metals in wastewater. Folia Microbiol 47(1):43–50

    Article  CAS  Google Scholar 

  • Shamuyarira KK, Gumbo JR (2014) Assessment of heavy metals in municipal sewage sludge: a case study of Limpopo Province, South Africa. Int J Environ Res Public Health 11:2569–2579

    Article  CAS  Google Scholar 

  • Sharma VK, Fei Liu F, Tolan S, Sohn M, Kim H, Oturan MA (2013) Oxidation of β-lactam antibiotics by ferrate (VI). Chem Eng J 221:446–451

    Article  CAS  Google Scholar 

  • Singh R, Gautam N, Mishra A, Gupta R (2011) Heavy metals and living systems: an overview. Indian J Pharmacol 43(3):246–253

    Article  CAS  Google Scholar 

  • Sivaprakasam S, Mahadevan S, Sekar S, Rajakumar S (2008) Biological treatment of tannery wastewater by using salt-tolerant bacterial strains. Microbial Cell Fact 7(15):1–7

    Google Scholar 

  • Smith RL, Maguire ME (1995) Distribution of the CorA Mg2+ transport system in gram-negative bacteria. J Bacteriol 177(6):1638–1640

    CAS  Google Scholar 

  • Sorensen SJ, Bailey M, Hansen LH, Kroer N, Wuertz S (2005) Studying plasmid horizontal transfer in situ: a critical review. Nat Rev Microbiol 3:700–771

    Article  CAS  Google Scholar 

  • Spongberg AL, Witter JD (2008) Pharmaceutical compounds in the wastewater process stream in Northwest Ohio. J Sci Environ 397(1–3):148–157

    CAS  Google Scholar 

  • Sternbeck J (2000) Behaviour and effects of copper in water and soil. IVL-Report. B1349. IVL Publications Service, Stockholm, p 29

  • Suemitsu R, Uenishi R, Akashi I, Nakano M (1986) The use of dyestuff-treated rice hulls for removal of heavy metals from wastewater. J Appl Poly Sci 31:74–83

    Article  Google Scholar 

  • Sukumar C, Janaki V, Kamala-Kannan S, Shanthi K (2014) Biosorption of chromium(VI) using Bacillus subtilis SS-1 isolated from soil samples of electroplating industry. Clean Technol Environ Policy 16:405–413. doi:10.1007/s10098-013-0636-0

    Article  CAS  Google Scholar 

  • Sundar K, Mukherjee A, Sadiq M, Chandrasekaran N (2011) Cr (III) bioremoval capacities of indigenous and adapted bacterial strains from Palar river basin. J Hazard Mater 187(1–3):553–561

    Article  CAS  Google Scholar 

  • Ternes TA, Joss A, Siegrist H (2004) Scrutinizing pharmaceuticals and personal care products in wastewater treatment. Environ Sci Technol 38(20):392–399

    Article  Google Scholar 

  • Toroglu S, Dincer S, Korkmaz H (2005) Antibiotic resistance in Gram-negative bacteria isolated from Aksu River in Turkey. Ann Microbiol 55:229–233

    CAS  Google Scholar 

  • Tsekova K, Todorova D, Dencheva V, Ganeva S (2010) Biosorption of copper (II) and cadmium (II) from aqueous solutions by free and immobilized biomass of A. niger. Biores Technol 101(6):1727–1731

    Article  CAS  Google Scholar 

  • Tsekova K, Christova D, Todorova D, Ivanova S (2011) Removal of Cu(II), Co(II) and Fe(III) ions from ternary solution by free and entrapped in PVA-hydrogel biomass of P. cyclopium. Biotechnol Equip 25(4):41–46

  • Tuomanen E, Durack DT, Tomasz A (1986) Antimicrobial tolerance among clinical isolates of bacteria. Antimicrob Agents Chemother 30:521–527

    Article  CAS  Google Scholar 

  • Tylová T, Flieger M, Olšovská J (2013) Determination of antibiotics in influents and effluents of wastewater-treatment-plants in the Czech Republic—development and application of the SPE and a UHPLC-ToFMS method. Anal Methods 5(8):2110–2118

    Article  CAS  Google Scholar 

  • U.S. EPA (2003) Control of pathogens and vector attraction in sewage sludge; 40 CFR Part 503. U.S. Environmental Protection Agency, Cincinnati

  • Velasquez L, Dussan J (2009) Biosorption and bioaccumulation of heavy metals on dead and living biomass of B. sphaericus. J Hazard Mater 167(1–3):713–716

    Google Scholar 

  • Velickovic-Radovanovic R, Petrovic J, Kocic B (2009) Correlation between antibiotic consumption and bacterial resistance as quality indicator of proper use of these drugs in inpatients. Vojnosanit Pregl 66(4):307–312

    Article  Google Scholar 

  • Vijayaraghavan K, Yun YS (2008) Bacterial biosorbents and biosorption. Biotechnol Adv 26(3):266–291

    Article  CAS  Google Scholar 

  • Vilanova X, Blanch AR (2005) Distribution and persistence of faecal bacterial populations in liquid and dewatered sludge from a biological treatment plant. J Gen Appl Microbiol 51(6):361–368

    Article  CAS  Google Scholar 

  • Vital M, Stucki D, Egli T, Hammes F (2010) Evaluating the growth potential of pathogenic bacteria in water. Appl Environ Microbiol 67(19):6477–6484

    Article  CAS  Google Scholar 

  • Volesky B, Weber J, Vieira RHSF (1999) Biosorption of Cd and Cu by different types of Sargassum biomass. In: Amils R, Ballester A (eds) Biohydrometallurgy and the environment towards the mining of 21st century (part B): international biohydrometallurgy symposium—Proceedings. Elsevier, Amsterdam, pp 473–482

  • Wang J, Chen C (2009) Biosorbents for heavy metals removal and their future. Biotechnol Adv 27(2):195–226

    Article  CAS  Google Scholar 

  • Watkinson AJ, Murbyc EJ, Costanzo SD (2007) Removal of antibiotics in conventional and advanced wastewater treatment: implications for environmental discharge and wastewater recycling. Water Res 41(18):4164–4176

    Article  CAS  Google Scholar 

  • Wernerus H (2002) Engineering of staphylococcal surfaces for biotechnological applications. Department of Biotechnology, Royal Institute of Technology, Stockholm

    Google Scholar 

  • WHO (1984) Guidelines for drinking water quality. World Health Organization, Geneva

    Google Scholar 

  • WHO (1995) Inorganic lead. Environmental Health Criteria 165. World Health Organisation, International Programme on Chemical Safety (IPCS), Geneva, Switzerland

  • WHO (2005) Nickel in drinking-water. Guidelines for drinking-water quality. World Health Organization, Geneva

    Google Scholar 

  • Wiuff C, Zappala RM, Regoes RR, Garner KN, Baquero F, Levin BR (2005) Phenotypic tolerance: antibiotic enrichment of non-inherited resistance in bacterial populations. Antimicrob Agents Chemother 49(4):1483–1494

    Article  CAS  Google Scholar 

  • Wnorowski AU (1991) Selection of bacterial and fungal strains for bioaccumulation of heavy metals from aqueous solutions. Water Sci Technol 23(1–3):309–318

    CAS  Google Scholar 

  • Wong JPK, Wong YS, Tam NFY (2000) Nickel biosorption by two Chlorella species, C. vulgaris (a commercial species) and C. miniata (a local isolate). Biores Technol 73:133–137

    Article  CAS  Google Scholar 

  • Wong JWC, Xiang L, Chan LC (2002) pH requirement for the bioleaching of heavy metals from an aerobically digested wastewater sludge. Water Air Soil Pollut 138:25–35

    Article  CAS  Google Scholar 

  • Wu C, Spongberg AL, Witter JD (2009) Sorption and biodegradation of selected antibiotics in biosolids. J Environ Sci Health A 44(5):454–461

    Article  CAS  Google Scholar 

  • Xu WH, Zhang G, Li XD, Zou SC, Li P, Hu ZH, Li J (2007) Occurrence and elimination of antibiotics at four sewage treatment plants in the Pearl River Delta (PRD). South China. Water Res 41(19):4526–4534

    Article  CAS  Google Scholar 

  • Yan GVY, Viraraghavan T (2000) Effect of pretreatment on the bioadsorption of heavy metals on M. rouxii. Water SA 26(1):119–123

    CAS  Google Scholar 

  • Yao H, Lu J, Wu J, Lu Z, Wilson PC, Shen Y (2013) Adsorption of fluoroquinolone antibiotics by wastewater sludge biochar: role of the sludge source. Water Air Soil Pollut 224:1370

    Article  CAS  Google Scholar 

  • Yargeau V, Leclair C (2007) Potential of ozonation for the degradation of antibiotics in wastewater. Water Sci Technol 55(12):321–326

    Article  CAS  Google Scholar 

  • Yoshimurat F, Nikaido H (1985) Diffusion of β-Lactam antibiotics through the porin channels of Escherichia coli K-12. Antimicrob Agents Chemother 27:84–92

    Article  Google Scholar 

  • Zhang T, Li B (2011) Occurrence, transformation, and fate of antibiotics in municipal wastewater treatment plants. Crit Rev Environ Sci Technol 41(11):951–998

    Article  CAS  Google Scholar 

  • Zhang XX, Zhang T, Fang H (2009) Antibiotic resistance genes in water environment. Appl Microbiol Biotechnol 82:397–414

    Article  CAS  Google Scholar 

  • Zhou L, Ying G, Liu S, Zhao J, Yang B, Chen Z, Lai H (2013) Occurrence and fate of eleven classes of antibiotics in two typical wastewater treatment plants in South China. Sci Total Environ 452–453:365–376

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge the fellowship by TWAS-USM, and financial support from the Ministry of Higher Education of Malaysia for the research project under fundamental research Grant scheme (FRGS) (203/PTEKIND/6711328).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ismail Norli.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Al-Gheethi, A.A.S., Lalung, J., Noman, E.A. et al. Removal of heavy metals and antibiotics from treated sewage effluent by bacteria. Clean Techn Environ Policy 17, 2101–2123 (2015). https://doi.org/10.1007/s10098-015-0968-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10098-015-0968-z

Keywords

Navigation